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1. Horizon scanning the application of probiotics for wildlife

Author: Garcias-Bonet, N, Roik, A, Tierney, B, Garcia, FC, Villela, HDM, Dungan, AM, Quigley, KM, Sweet, M, Berg, G, Gram, L, Bourne, DG, Ushijima, B, Sogin, M, Hoj, L, Duarte, G, Hirt, H, Smalla, K, Rosado, AS, Carvalho, S, Thurber, RV, Ziegler, M, Mason, CE, van Oppen, MJH, Voolstra, CR, Peixoto, RS, Garcias-Bonet, N, Roik, A, Tierney, B, Garcia, FC, Villela, HDM, Dungan, AM, Quigley, KM, Sweet, M, Berg, G, Gram, L, Bourne, DG, Ushijima, B, Sogin, M, Hoj, L, Duarte, G, Hirt, H, Smalla, K, Rosado, AS, Carvalho, S, Thurber, RV, Ziegler, M, Mason, CE, van Oppen, MJH, Voolstra, CR, and Peixoto, RS
Abstract: The provision of probiotics benefits the health of a wide range of organisms, from humans to animals and plants. Probiotics can enhance stress resilience of endangered organisms, many of which are critically threatened by anthropogenic impacts. The use of so-called 'probiotics for wildlife' is a nascent application, and the field needs to reflect on standards for its development, testing, validation, risk assessment, and deployment. Here, we identify the main challenges of this emerging intervention and provide a roadmap to validate the effectiveness of wildlife probiotics. We cover the essential use of inert negative controls in trials and the investigation of the probiotic mechanisms of action. We also suggest alternative microbial therapies that could be tested in parallel with the probiotic application. Our recommendations align approaches used for humans, aquaculture, and plants to the emerging concept and use of probiotics for wildlife.
Published: 2024

2. Building consensus around the assessment and interpretation of Symbiodiniaceae diversity.

Author: Davies, SW, Gamache, MH, Howe-Kerr, LI, Kriefall, NG, Baker, AC, Banaszak, AT, Bay, LK, Bellantuono, AJ, Bhattacharya, D, Chan, CX, Claar, DC, Coffroth, MA, Cunning, R, Davy, SK, Del Campo, J, Díaz-Almeyda, EM, Frommlet, JC, Fuess, LE, González-Pech, RA, Goulet, TL, Hoadley, KD, Howells, EJ, Hume, BCC, Kemp, DW, Kenkel, CD, Kitchen, SA, LaJeunesse, TC, Lin, S, McIlroy, SE, McMinds, R, Nitschke, MR, Oakley, CA, Peixoto, RS, Prada, C, Putnam, HM, Quigley, K, Reich, HG, Reimer, JD, Rodriguez-Lanetty, M, Rosales, SM, Saad, OS, Sampayo, EM, Santos, SR, Shoguchi, E, Smith, EG, Stat, M, Stephens, TG, Strader, ME, Suggett, DJ, Swain, TD, Tran, C, Traylor-Knowles, N, Voolstra, CR, Warner, ME, Weis, VM, Wright, RM, Xiang, T, Yamashita, H, Ziegler, M, Correa, AMS, Parkinson, JE, Davies, SW, Gamache, MH, Howe-Kerr, LI, Kriefall, NG, Baker, AC, Banaszak, AT, Bay, LK, Bellantuono, AJ, Bhattacharya, D, Chan, CX, Claar, DC, Coffroth, MA, Cunning, R, Davy, SK, Del Campo, J, Díaz-Almeyda, EM, Frommlet, JC, Fuess, LE, González-Pech, RA, Goulet, TL, Hoadley, KD, Howells, EJ, Hume, BCC, Kemp, DW, Kenkel, CD, Kitchen, SA, LaJeunesse, TC, Lin, S, McIlroy, SE, McMinds, R, Nitschke, MR, Oakley, CA, Peixoto, RS, Prada, C, Putnam, HM, Quigley, K, Reich, HG, Reimer, JD, Rodriguez-Lanetty, M, Rosales, SM, Saad, OS, Sampayo, EM, Santos, SR, Shoguchi, E, Smith, EG, Stat, M, Stephens, TG, Strader, ME, Suggett, DJ, Swain, TD, Tran, C, Traylor-Knowles, N, Voolstra, CR, Warner, ME, Weis, VM, Wright, RM, Xiang, T, Yamashita, H, Ziegler, M, Correa, AMS, and Parkinson, JE
Abstract: Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.
Published: 2023

3. Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia.

Author: Cui, G, Konciute, MK, Ling, L, Esau, L, Raina, J-B, Han, B, Salazar, OR, Presnell, JS, Rädecker, N, Zhong, H, Menzies, J, Cleves, PA, Liew, YJ, Krediet, CJ, Sawiccy, V, Cziesielski, MJ, Guagliardo, P, Bougoure, J, Pernice, M, Hirt, H, Voolstra, CR, Weis, VM, Pringle, JR, Aranda, M, Cui, G, Konciute, MK, Ling, L, Esau, L, Raina, J-B, Han, B, Salazar, OR, Presnell, JS, Rädecker, N, Zhong, H, Menzies, J, Cleves, PA, Liew, YJ, Krediet, CJ, Sawiccy, V, Cziesielski, MJ, Guagliardo, P, Bougoure, J, Pernice, M, Hirt, H, Voolstra, CR, Weis, VM, Pringle, JR, and Aranda, M
Abstract: Symbiotic cnidarians such as corals and anemones form highly productive and biodiverse coral reef ecosystems in nutrient-poor ocean environments, a phenomenon known as Darwin's paradox. Resolving this paradox requires elucidating the molecular bases of efficient nutrient distribution and recycling in the cnidarian-dinoflagellate symbiosis. Using the sea anemone Aiptasia, we show that during symbiosis, the increased availability of glucose and the presence of the algae jointly induce the coordinated up-regulation and relocalization of glucose and ammonium transporters. These molecular responses are critical to support symbiont functioning and organism-wide nitrogen assimilation through glutamine synthetase/glutamate synthase-mediated amino acid biosynthesis. Our results reveal crucial aspects of the molecular mechanisms underlying nitrogen conservation and recycling in these organisms that allow them to thrive in the nitrogen-poor ocean environments.
Published: 2023

4. Building consensus around the assessment and interpretation of Symbiodiniaceae diversity.

Author: Davies, SW, Gamache, MH, Howe-Kerr, LI, Kriefall, NG, Baker, AC, Banaszak, AT, Bay, LK, Bellantuono, AJ, Bhattacharya, D, Chan, CX, Claar, DC, Coffroth, MA, Cunning, R, Davy, SK, Del Campo, J, Díaz-Almeyda, EM, Frommlet, JC, Fuess, LE, González-Pech, RA, Goulet, TL, Hoadley, KD, Howells, EJ, Hume, BCC, Kemp, DW, Kenkel, CD, Kitchen, SA, LaJeunesse, TC, Lin, S, McIlroy, SE, McMinds, R, Nitschke, MR, Oakley, CA, Peixoto, RS, Prada, C, Putnam, HM, Quigley, K, Reich, HG, Reimer, JD, Rodriguez-Lanetty, M, Rosales, SM, Saad, OS, Sampayo, EM, Santos, SR, Shoguchi, E, Smith, EG, Stat, M, Stephens, TG, Strader, ME, Suggett, DJ, Swain, TD, Tran, C, Traylor-Knowles, N, Voolstra, CR, Warner, ME, Weis, VM, Wright, RM, Xiang, T, Yamashita, H, Ziegler, M, Correa, AMS, Parkinson, JE, Davies, SW, Gamache, MH, Howe-Kerr, LI, Kriefall, NG, Baker, AC, Banaszak, AT, Bay, LK, Bellantuono, AJ, Bhattacharya, D, Chan, CX, Claar, DC, Coffroth, MA, Cunning, R, Davy, SK, Del Campo, J, Díaz-Almeyda, EM, Frommlet, JC, Fuess, LE, González-Pech, RA, Goulet, TL, Hoadley, KD, Howells, EJ, Hume, BCC, Kemp, DW, Kenkel, CD, Kitchen, SA, LaJeunesse, TC, Lin, S, McIlroy, SE, McMinds, R, Nitschke, MR, Oakley, CA, Peixoto, RS, Prada, C, Putnam, HM, Quigley, K, Reich, HG, Reimer, JD, Rodriguez-Lanetty, M, Rosales, SM, Saad, OS, Sampayo, EM, Santos, SR, Shoguchi, E, Smith, EG, Stat, M, Stephens, TG, Strader, ME, Suggett, DJ, Swain, TD, Tran, C, Traylor-Knowles, N, Voolstra, CR, Warner, ME, Weis, VM, Wright, RM, Xiang, T, Yamashita, H, Ziegler, M, Correa, AMS, and Parkinson, JE
Abstract: Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.
Published: 2023

5. Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia.

Author: Cui, G, Konciute, MK, Ling, L, Esau, L, Raina, J-B, Han, B, Salazar, OR, Presnell, JS, Rädecker, N, Zhong, H, Menzies, J, Cleves, PA, Liew, YJ, Krediet, CJ, Sawiccy, V, Cziesielski, MJ, Guagliardo, P, Bougoure, J, Pernice, M, Hirt, H, Voolstra, CR, Weis, VM, Pringle, JR, Aranda, M, Cui, G, Konciute, MK, Ling, L, Esau, L, Raina, J-B, Han, B, Salazar, OR, Presnell, JS, Rädecker, N, Zhong, H, Menzies, J, Cleves, PA, Liew, YJ, Krediet, CJ, Sawiccy, V, Cziesielski, MJ, Guagliardo, P, Bougoure, J, Pernice, M, Hirt, H, Voolstra, CR, Weis, VM, Pringle, JR, and Aranda, M
Abstract: Symbiotic cnidarians such as corals and anemones form highly productive and biodiverse coral reef ecosystems in nutrient-poor ocean environments, a phenomenon known as Darwin's paradox. Resolving this paradox requires elucidating the molecular bases of efficient nutrient distribution and recycling in the cnidarian-dinoflagellate symbiosis. Using the sea anemone Aiptasia, we show that during symbiosis, the increased availability of glucose and the presence of the algae jointly induce the coordinated up-regulation and relocalization of glucose and ammonium transporters. These molecular responses are critical to support symbiont functioning and organism-wide nitrogen assimilation through glutamine synthetase/glutamate synthase-mediated amino acid biosynthesis. Our results reveal crucial aspects of the molecular mechanisms underlying nitrogen conservation and recycling in these organisms that allow them to thrive in the nitrogen-poor ocean environments.
Published: 2023

6. Deoxygenation lowers the thermal threshold of coral bleaching.

Author: Alderdice, R, Perna, G, Cárdenas, A, Hume, BCC, Wolf, M, Kühl, M, Pernice, M, Suggett, DJ, Voolstra, CR, Alderdice, R, Perna, G, Cárdenas, A, Hume, BCC, Wolf, M, Kühl, M, Pernice, M, Suggett, DJ, and Voolstra, CR
Abstract: Exposure to deoxygenation from climate warming and pollution is emerging as a contributing factor of coral bleaching and mortality. However, the combined effects of heating and deoxygenation on bleaching susceptibility remain unknown. Here, we employed short-term thermal stress assays to show that deoxygenated seawater can lower the thermal limit of an Acropora coral by as much as 1 °C or 0.4 °C based on bleaching index scores or dark-acclimated photosynthetic efficiencies, respectively. Using RNA-Seq, we show similar stress responses to heat with and without deoxygenated seawater, both activating putative key genes of the hypoxia-inducible factor response system indicative of cellular hypoxia. We also detect distinct deoxygenation responses, including a disruption of O2-dependent photo-reception/-protection, redox status, and activation of an immune response prior to the onset of bleaching. Thus, corals are even more vulnerable when faced with heat stress in deoxygenated waters. This highlights the need to integrate dissolved O2 measurements into global monitoring programs of coral reefs.
Published: 2022

7. Widespread oxyregulation in tropical corals under hypoxia

Author: Hughes, DJ, Alexander, J, Cobbs, G, Kühl, M, Cooney, C, Pernice, M, Varkey, D, Voolstra, CR, Suggett, DJ, Hughes, DJ, Alexander, J, Cobbs, G, Kühl, M, Cooney, C, Pernice, M, Varkey, D, Voolstra, CR, and Suggett, DJ
Published: 2022

8. Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling.

Author: Rädecker, N, Pogoreutz, C, Gegner, HM, Cárdenas, A, Perna, G, Geißler, L, Roth, F, Bougoure, J, Guagliardo, P, Struck, U, Wild, C, Pernice, M, Raina, J-B, Meibom, A, Voolstra, CR, Rädecker, N, Pogoreutz, C, Gegner, HM, Cárdenas, A, Perna, G, Geißler, L, Roth, F, Bougoure, J, Guagliardo, P, Struck, U, Wild, C, Pernice, M, Raina, J-B, Meibom, A, and Voolstra, CR
Abstract: Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.
Published: 2022

9. Greater functional diversity and redundancy of coral endolithic microbiomes align with lower coral bleaching susceptibility.

Author: Cárdenas, A, Raina, J-B, Pogoreutz, C, Rädecker, N, Bougoure, J, Guagliardo, P, Pernice, M, Voolstra, CR, Cárdenas, A, Raina, J-B, Pogoreutz, C, Rädecker, N, Bougoure, J, Guagliardo, P, Pernice, M, and Voolstra, CR
Abstract: The skeleton of reef-building coral harbors diverse microbial communities that could compensate for metabolic deficiencies caused by the loss of algal endosymbionts, i.e., coral bleaching. However, it is unknown to what extent endolith taxonomic diversity and functional potential might contribute to thermal resilience. Here we exposed Goniastrea edwardsi and Porites lutea, two common reef-building corals from the central Red Sea to a 17-day long heat stress. Using hyperspectral imaging, marker gene/metagenomic sequencing, and NanoSIMS, we characterized their endolithic microbiomes together with 15N and 13C assimilation of two skeletal compartments: the endolithic band directly below the coral tissue and the deep skeleton. The bleaching-resistant G. edwardsi was associated with endolithic microbiomes of greater functional diversity and redundancy that exhibited lower N and C assimilation than endoliths in the bleaching-sensitive P. lutea. We propose that the lower endolithic primary productivity in G. edwardsi can be attributed to the dominance of chemolithotrophs. Lower primary production within the skeleton may prevent unbalanced nutrient fluxes to coral tissues under heat stress, thereby preserving nutrient-limiting conditions characteristic of a stable coral-algal symbiosis. Our findings link coral endolithic microbiome structure and function to bleaching susceptibility, providing new avenues for understanding and eventually mitigating reef loss.
Published: 2022

10. Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling.

Author: Rädecker, N, Pogoreutz, C, Gegner, HM, Cárdenas, A, Perna, G, Geißler, L, Roth, F, Bougoure, J, Guagliardo, P, Struck, U, Wild, C, Pernice, M, Raina, J-B, Meibom, A, Voolstra, CR, Rädecker, N, Pogoreutz, C, Gegner, HM, Cárdenas, A, Perna, G, Geißler, L, Roth, F, Bougoure, J, Guagliardo, P, Struck, U, Wild, C, Pernice, M, Raina, J-B, Meibom, A, and Voolstra, CR
Abstract: Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.
Published: 2022

11. Widespread oxyregulation in tropical corals under hypoxia

Author: Hughes, DJ, Alexander, J, Cobbs, G, Kühl, M, Cooney, C, Pernice, M, Varkey, D, Voolstra, CR, Suggett, DJ, Hughes, DJ, Alexander, J, Cobbs, G, Kühl, M, Cooney, C, Pernice, M, Varkey, D, Voolstra, CR, and Suggett, DJ
Published: 2022

12. Disparate Inventories of Hypoxia Gene Sets Across Corals Align With Inferred Environmental Resilience

Author: Alderdice, R, Hume, BCC, Kühl, M, Pernice, M, Suggett, DJ, Voolstra, CR, Alderdice, R, Hume, BCC, Kühl, M, Pernice, M, Suggett, DJ, and Voolstra, CR
Abstract: Aquatic deoxygenation has been flagged as an overlooked but key factor contributing to mass bleaching-induced coral mortality. During deoxygenation events triggered by coastal nutrient pollution and ocean warming, oxygen supplies lower to concentrations that can elicit an aerobic metabolic crisis i.e., hypoxia. Surprisingly little is known of the fundamental hypoxia gene set inventory that corals possess to respond to lowered oxygen (i.e., deoxygenation). For instance, it is unclear whether gene copy number differences exist across species that may affect the efficacy of a measured transcriptomic stress response. Therefore, we conducted an ortholog-based meta-analysis to investigate how hypoxia gene inventories differ amongst coral species to assess putative copy number variations (CNVs). We specifically elucidated CNVs for a compiled list of 32 hypoxia genes across 24 protein sets from species with a sequenced genome spanning corals from the robust and complex clade. We found approximately a third of the investigated genes exhibited copy number differences, and these differences were species-specific rather than attributable to the robust-complex split. Interestingly, we consistently found the highest gene expansion present in Porites lutea, which is considered to exhibit inherently greater stress tolerance than other species. Consequently, our analysis suggests that hypoxia stress gene expansion may coincide with increased stress tolerance. As such, the unevenly expanded (or reduced) hypoxia genes presented here provide key genes of interest to target in examining (or diagnosing) coral stress responses. Important next steps will involve determining to what extent such gene copy differences align with certain coral traits.
Published: 2022

13. Disparate Inventories of Hypoxia Gene Sets Across Corals Align With Inferred Environmental Resilience

Author: Alderdice, R, Hume, BCC, Kühl, M, Pernice, M, Suggett, DJ, Voolstra, CR, Alderdice, R, Hume, BCC, Kühl, M, Pernice, M, Suggett, DJ, and Voolstra, CR
Abstract: Aquatic deoxygenation has been flagged as an overlooked but key factor contributing to mass bleaching-induced coral mortality. During deoxygenation events triggered by coastal nutrient pollution and ocean warming, oxygen supplies lower to concentrations that can elicit an aerobic metabolic crisis i.e., hypoxia. Surprisingly little is known of the fundamental hypoxia gene set inventory that corals possess to respond to lowered oxygen (i.e., deoxygenation). For instance, it is unclear whether gene copy number differences exist across species that may affect the efficacy of a measured transcriptomic stress response. Therefore, we conducted an ortholog-based meta-analysis to investigate how hypoxia gene inventories differ amongst coral species to assess putative copy number variations (CNVs). We specifically elucidated CNVs for a compiled list of 32 hypoxia genes across 24 protein sets from species with a sequenced genome spanning corals from the robust and complex clade. We found approximately a third of the investigated genes exhibited copy number differences, and these differences were species-specific rather than attributable to the robust-complex split. Interestingly, we consistently found the highest gene expansion present in Porites lutea, which is considered to exhibit inherently greater stress tolerance than other species. Consequently, our analysis suggests that hypoxia stress gene expansion may coincide with increased stress tolerance. As such, the unevenly expanded (or reduced) hypoxia genes presented here provide key genes of interest to target in examining (or diagnosing) coral stress responses. Important next steps will involve determining to what extent such gene copy differences align with certain coral traits.
Published: 2022

14. Deoxygenation lowers the thermal threshold of coral bleaching.

Author: Alderdice, R, Perna, G, Cárdenas, A, Hume, BCC, Wolf, M, Kühl, M, Pernice, M, Suggett, DJ, Voolstra, CR, Alderdice, R, Perna, G, Cárdenas, A, Hume, BCC, Wolf, M, Kühl, M, Pernice, M, Suggett, DJ, and Voolstra, CR
Abstract: Exposure to deoxygenation from climate warming and pollution is emerging as a contributing factor of coral bleaching and mortality. However, the combined effects of heating and deoxygenation on bleaching susceptibility remain unknown. Here, we employed short-term thermal stress assays to show that deoxygenated seawater can lower the thermal limit of an Acropora coral by as much as 1 °C or 0.4 °C based on bleaching index scores or dark-acclimated photosynthetic efficiencies, respectively. Using RNA-Seq, we show similar stress responses to heat with and without deoxygenated seawater, both activating putative key genes of the hypoxia-inducible factor response system indicative of cellular hypoxia. We also detect distinct deoxygenation responses, including a disruption of O2-dependent photo-reception/-protection, redox status, and activation of an immune response prior to the onset of bleaching. Thus, corals are even more vulnerable when faced with heat stress in deoxygenated waters. This highlights the need to integrate dissolved O2 measurements into global monitoring programs of coral reefs.
Published: 2022

15. Heat stress destabilizes symbiotic nutrient cycling in corals

Author: Rädecker, N, Pogoreutz, C, Gegner, HM, Cárdenas, A, Roth, F, Bougoure, J, Guagliardo, P, Wild, C, Pernice, M, Raina, J-B, Meibom, A, Voolstra, CR, Rädecker, N, Pogoreutz, C, Gegner, HM, Cárdenas, A, Roth, F, Bougoure, J, Guagliardo, P, Wild, C, Pernice, M, Raina, J-B, Meibom, A, and Voolstra, CR
Abstract: Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral–algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral–algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral–algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.
Published: 2021

16. Projecting coral responses to intensifying marine heatwaves under ocean acidification

Author: Klein, SG, Geraldi, NR, Anton, A, Schmidt‐Roach, S, Ziegler, M, Cziesielski, MJ, Martin, C, Rädecker, N, Frölicher, TL, Mumby, PJ, Pandolfi, JM, Suggett, DJ, Voolstra, CR, Aranda, M, Duarte, CM, Klein, SG, Geraldi, NR, Anton, A, Schmidt‐Roach, S, Ziegler, M, Cziesielski, MJ, Martin, C, Rädecker, N, Frölicher, TL, Mumby, PJ, Pandolfi, JM, Suggett, DJ, Voolstra, CR, Aranda, M, and Duarte, CM
Abstract: Over this century, coral reefs will run the gauntlet of climate change, as marine heatwaves (MHWs) become more intense and frequent, and ocean acidification (OA) progresses. However, we still lack a quantitative assessment of how, and to what degree, OA will moderate the responses of corals to MHWs as they intensify throughout this century. Here, we first projected future MHW intensities for tropical regions under three future greenhouse gas emissions scenario (representative concentration pathways, RCP2.6, RCP4.5 and RCP8.5) for the near-term (2021-2040), mid-century (2041-2060) and late-century (2081-2100). We then combined these MHW intensity projections with a global data set of 1,788 experiments to assess coral attribute performance and survival under the three emissions scenarios for the near-term, mid-century and late-century in the presence and absence of OA. Although warming and OA had predominately additive impacts on the coral responses, the contribution of OA in affecting most coral attributes was minor relative to the dominant role of intensifying MHWs. However, the addition of OA led to greater decreases in photosynthesis and survival under intermediate and unrestricted emissions scenario for the mid- and late-century than if intensifying MHWs were considered as the only driver. These results show that role of OA in modulating coral responses to intensifying MHWs depended on the focal coral attribute and extremity of the scenario examined. Specifically, intensifying MHWs and OA will cause increasing instances of coral bleaching and substantial declines in coral productivity, calcification and survival within the next two decades under the low and intermediate emissions scenario. These projections suggest that corals must rapidly adapt or acclimatize to projected ocean conditions to persist, which is far more likely under a low emissions scenario and with increasing efforts to manage reefs to enhance resilience.
Published: 2021

17. Integrating environmental variability to broaden the research on coral responses to future ocean conditions

Author: Ziegler, M, Anton, A, Klein, SG, Rädecker, N, Geraldi, NR, Schmidt‐Roach, S, Saderne, V, Mumby, PJ, Cziesielski, MJ, Martin, C, Frölicher, TL, Pandolfi, JM, Suggett, DJ, Aranda, M, Duarte, CM, Voolstra, CR, Ziegler, M, Anton, A, Klein, SG, Rädecker, N, Geraldi, NR, Schmidt‐Roach, S, Saderne, V, Mumby, PJ, Cziesielski, MJ, Martin, C, Frölicher, TL, Pandolfi, JM, Suggett, DJ, Aranda, M, Duarte, CM, and Voolstra, CR
Abstract: Our understanding of the response of reef-building corals to changes in their physical environment is largely based on laboratory experiments, analysis of long-term field data, and model projections. Experimental data provide unique insights into how organisms respond to variation of environmental drivers. However, an assessment of how well experimental conditions cover the breadth of environmental conditions and variability where corals live successfully is missing. Here, we compiled and analyzed a globally distributed dataset of in-situ seasonal and diurnal variability of key environmental drivers (temperature, pCO2 , and O2 ) critical for the growth and livelihood of reef-building corals. Using a meta-analysis approach, we compared the variability of environmental conditions assayed in coral experimental studies to current and projected conditions in their natural habitats. We found that annual temperature profiles projected for the end of the 21st century were characterized by distributional shifts in temperatures with warmer winters and longer warm periods in the summer, not just peak temperatures. Furthermore, short-term hourly fluctuations of temperature and pCO2 may regularly expose corals to conditions beyond the projected average increases for the end of the 21st century. Coral reef sites varied in the degree of coupling between temperature, pCO2 , and dissolved O2 , which warrants site-specific, differentiated experimental approaches depending on the local hydrography and influence of biological processes on the carbonate system and O2 availability. Our analysis highlights that a large portion of the natural environmental variability at short and long timescales is underexplored in experimental designs, which may provide a path to extend our understanding on the response of corals to global climate change.
Published: 2021

18. Consensus Guidelines for Advancing Coral Holobiont Genome and Specimen Voucher Deposition

Author: Voolstra, CR, Quigley, KM, Davies, SW, Parkinson, JE, Peixoto, RS, Aranda, M, Baker, AC, Barno, AR, Barshis, DJ, Benzoni, F, Bonito, V, Bourne, DG, Buitrago-López, C, Bridge, TCL, Chan, CX, Combosch, DJ, Craggs, J, Frommlet, JC, Herrera, S, Quattrini, AM, Röthig, T, Reimer, JD, Rubio-Portillo, E, Suggett, DJ, Villela, H, Ziegler, M, Sweet, M, Voolstra, CR, Quigley, KM, Davies, SW, Parkinson, JE, Peixoto, RS, Aranda, M, Baker, AC, Barno, AR, Barshis, DJ, Benzoni, F, Bonito, V, Bourne, DG, Buitrago-López, C, Bridge, TCL, Chan, CX, Combosch, DJ, Craggs, J, Frommlet, JC, Herrera, S, Quattrini, AM, Röthig, T, Reimer, JD, Rubio-Portillo, E, Suggett, DJ, Villela, H, Ziegler, M, and Sweet, M
Abstract: Coral research is being ushered into the genomic era. To fully capitalize on the potential discoveries from this genomic revolution, the rapidly increasing number of high-quality genomes requires effective pairing with rigorous taxonomic characterizations of specimens and the contextualization of their ecological relevance. However, to date there is no formal framework that genomicists, taxonomists, and coral scientists can collectively use to systematically acquire and link these data. Spurred by the recently announced “Coral symbiosis sensitivity to environmental change hub” under the “Aquatic Symbiosis Genomics Project” - a collaboration between the Wellcome Sanger Institute and the Gordon and Betty Moore Foundation to generate gold-standard genome sequences for coral animal hosts and their associated Symbiodiniaceae microalgae (among the sequencing of many other symbiotic aquatic species) - we outline consensus guidelines to reconcile different types of data. The metaorganism nature of the coral holobiont provides a particular challenge in this context and is a key factor to consider for developing a framework to consolidate genomic, taxonomic, and ecological (meta)data. Ideally, genomic data should be accompanied by taxonomic references, i.e., skeletal vouchers as formal morphological references for corals and strain specimens in the case of microalgal and bacterial symbionts (cultured isolates). However, exhaustive taxonomic characterization of all coral holobiont member species is currently not feasible simply because we do not have a comprehensive understanding of all the organisms that constitute the coral holobiont. Nevertheless, guidelines on minimal, recommended, and ideal-case descriptions for the major coral holobiont constituents (coral animal, Symbiodiniaceae microalgae, and prokaryotes) will undoubtedly help in future referencing and will facilitate comparative studies. We hope that the guidelines outlined here, which we will adhere to as part of th
Published: 2021

19. Extending the natural adaptive capacity of coral holobionts

Author: Voolstra, CR, Suggett, DJ, Peixoto, RS, Parkinson, JE, Quigley, KM, Silveira, CB, Sweet, M, Muller, EM, Barshis, DJ, Bourne, DG, Aranda, M, Voolstra, CR, Suggett, DJ, Peixoto, RS, Parkinson, JE, Quigley, KM, Silveira, CB, Sweet, M, Muller, EM, Barshis, DJ, Bourne, DG, and Aranda, M
Abstract: Anthropogenic climate change and environmental degradation destroy coral reefs, the ecosystem services they provide, and the livelihoods of close to a billion people who depend on these services. Restoration approaches to increase the resilience of corals are therefore necessary to counter environmental pressures relevant to climate change projections. In this Review, we examine the natural processes that can increase the adaptive capacity of coral holobionts, with the aim of preserving ecosystem functioning under future ocean conditions. Current approaches that centre around restoring reef cover can be integrated with emerging approaches to enhance coral stress resilience and, thereby, allow reefs to regrow under a new set of environmental conditions. Emerging approaches such as standardized acute thermal stress assays, selective sexual propagation, coral probiotics, and environmental hardening could be feasible and scalable in the real world. However, they must follow decision-making criteria that consider the different reef, environmental, and ecological conditions. The implementation of adaptive interventions tailored around nature-based solutions will require standardized frameworks, appropriate ecological risk–benefit assessments, and analytical routines for consistent and effective utilization and global coordination.
Published: 2021

20. Heat stress destabilizes symbiotic nutrient cycling in corals

Author: Rädecker, N, Pogoreutz, C, Gegner, HM, Cárdenas, A, Roth, F, Bougoure, J, Guagliardo, P, Wild, C, Pernice, M, Raina, J-B, Meibom, A, Voolstra, CR, Rädecker, N, Pogoreutz, C, Gegner, HM, Cárdenas, A, Roth, F, Bougoure, J, Guagliardo, P, Wild, C, Pernice, M, Raina, J-B, Meibom, A, and Voolstra, CR
Abstract: Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral–algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral–algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral–algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.
Published: 2021

21. Erratum: Correction to: Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities (Microbiome (2020) 8 1 (8))

Author: Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME, Smith, DJ, Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME, and Smith, DJ
Abstract: Following publication of the original article [1], the authors reported an error on the legend of of P.damicornis in Fig. 1.
Published: 2020

22. Increasing comparability among coral bleaching experiments.

Author: Grottoli AG, Toonen RJ, van Woesik R, Vega Thurber R, Warner ME, McLachlan RH, Price JT, Bahr KD, Baums IB, Castillo K, Coffroth MA, Cunning R, Dobson K, Donahue M, Hench JL, Iglesias-Prieto R, Kemp DW, Kenkel CD, Kline DI, Kuffner IB, Matthews JL, Mayfield A, Padilla-Gamino J, Palumbi S, Voolstra CR, Weis VM, Wu HC, Grottoli AG, Toonen RJ, van Woesik R, Vega Thurber R, Warner ME, McLachlan RH, Price JT, Bahr KD, Baums IB, Castillo K, Coffroth MA, Cunning R, Dobson K, Donahue M, Hench JL, Iglesias-Prieto R, Kemp DW, Kenkel CD, Kline DI, Kuffner IB, Matthews JL, Mayfield A, Padilla-Gamino J, Palumbi S, Voolstra CR, Weis VM, and Wu HC
Abstract: Coral bleaching is the single largest global threat to coral reefs worldwide. Integrating the diverse body of work on coral bleaching is critical to understanding and combating this global problem. Yet investigating the drivers, patterns, and processes of coral bleaching poses a major challenge. A recent review of published experiments revealed a wide range of experimental variables used across studies. Such a wide range of approaches enhances discovery, but without full transparency in the experimental and analytical methods used, can also make comparisons among studies challenging. To increase comparability but not stifle innovation, we propose a common framework for coral bleaching experiments that includes consideration of coral provenance, experimental conditions, and husbandry. For example, reporting the number of genets used, collection site conditions, the experimental temperature offset(s) from the maximum monthly mean (MMM) of the collection site, experimental light conditions, flow, and the feeding regime will greatly facilitate comparability across studies. Similarly, quantifying common response variables of endosymbiont (Symbiodiniaceae) and holobiont phenotypes (i.e., color, chlorophyll, endosymbiont cell density, mortality, and skeletal growth) could further facilitate cross-study comparisons. While no single bleaching experiment can provide the data necessary to determine global coral responses of all corals to current and future ocean warming, linking studies through a common framework as outlined here, would help increase comparability among experiments, facilitate synthetic insights into the causes and underlying mechanisms of coral bleaching, and reveal unique bleaching responses among genets, species, and regions. Such a collaborative framework that fosters transparency in methods used would strengthen comparisons among studies that can help inform coral reef management and facilitate conservation strategies to mitigate coral bleaching worldwide
Published: 2020

23. Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment

Author: Camp EF, Suggett DJ, Pogoreutz C, Nitschke MR, Houlbreque F, Hume BCC, Gardner SG, Zampighi M, Rodolfo-Metalpa R, Voolstra CR, Camp EF, Suggett DJ, Pogoreutz C, Nitschke MR, Houlbreque F, Hume BCC, Gardner SG, Zampighi M, Rodolfo-Metalpa R, and Voolstra CR
Abstract: © 2020, Springer-Verlag GmbH Germany, part of Springer Nature. Climate change threatens the survival of scleractinian coral from exposure to concurrent ocean warming, acidification and deoxygenation; how corals can potentially adapt to this trio of stressors is currently unknown. This study investigates three coral species (Acropora muricata, Acropora pulchra and Porites lutea) dominant in an extreme mangrove lagoon (Bouraké, New Caledonia) where abiotic conditions exceed those predicted for many reef sites over the next 100 years under climate change and compared them to conspecifics from an environmentally more benign reef habitat. We studied holobiont physiology as well as plasticity in coral-associated microorganisms (Symbiodiniaceae and bacteria) through ITS2 and 16S rRNA sequencing, respectively. We hypothesised that differences in coral-associated microorganisms (Symbiodiniaceae and bacteria) between the lagoonal and adjacent reef habitats may support coral host productivity and ultimately the ability of corals to live in extreme environments. In the lagoon, all coral species exhibited a metabolic adjustment of reduced photosynthesis-to-respiration ratios (P/R), but this was accompanied by highly divergent coral host-specific microbial associations. This was substantiated by the absence of shared ITS2-type profiles (proxies for Symbiodiniaceae genotypes). We observed that ITS2 profiles originating from Durusdinium taxa made up < 3% and a novel Symbiodinium ITS2 profile A1-A1v associated with A. pulchra. Bacterial community profiles were also highly divergent in corals from the lagoonal environment, whereas corals from the reef site were consistently dominated by Hahellaceae, Endozoicomonas. As such, differences in host–microorganism associations aligned with different physiologies and habitats. Our results argue that a multitude of host–microorganism associations are required to fulfill the changing nutritional demands of corals persisting into environments t
Published: 2020

24. Increasing comparability among coral bleaching experiments.

Author: Grottoli AG, Toonen RJ, van Woesik R, Vega Thurber R, Warner ME, McLachlan RH, Price JT, Bahr KD, Baums IB, Castillo K, Coffroth MA, Cunning R, Dobson K, Donahue M, Hench JL, Iglesias-Prieto R, Kemp DW, Kenkel CD, Kline DI, Kuffner IB, Matthews JL, Mayfield A, Padilla-Gamino J, Palumbi S, Voolstra CR, Weis VM, Wu HC, Grottoli AG, Toonen RJ, van Woesik R, Vega Thurber R, Warner ME, McLachlan RH, Price JT, Bahr KD, Baums IB, Castillo K, Coffroth MA, Cunning R, Dobson K, Donahue M, Hench JL, Iglesias-Prieto R, Kemp DW, Kenkel CD, Kline DI, Kuffner IB, Matthews JL, Mayfield A, Padilla-Gamino J, Palumbi S, Voolstra CR, Weis VM, and Wu HC
Abstract: Coral bleaching is the single largest global threat to coral reefs worldwide. Integrating the diverse body of work on coral bleaching is critical to understanding and combating this global problem. Yet investigating the drivers, patterns, and processes of coral bleaching poses a major challenge. A recent review of published experiments revealed a wide range of experimental variables used across studies. Such a wide range of approaches enhances discovery, but without full transparency in the experimental and analytical methods used, can also make comparisons among studies challenging. To increase comparability but not stifle innovation, we propose a common framework for coral bleaching experiments that includes consideration of coral provenance, experimental conditions, and husbandry. For example, reporting the number of genets used, collection site conditions, the experimental temperature offset(s) from the maximum monthly mean (MMM) of the collection site, experimental light conditions, flow, and the feeding regime will greatly facilitate comparability across studies. Similarly, quantifying common response variables of endosymbiont (Symbiodiniaceae) and holobiont phenotypes (i.e., color, chlorophyll, endosymbiont cell density, mortality, and skeletal growth) could further facilitate cross-study comparisons. While no single bleaching experiment can provide the data necessary to determine global coral responses of all corals to current and future ocean warming, linking studies through a common framework as outlined here, would help increase comparability among experiments, facilitate synthetic insights into the causes and underlying mechanisms of coral bleaching, and reveal unique bleaching responses among genets, species, and regions. Such a collaborative framework that fosters transparency in methods used would strengthen comparisons among studies that can help inform coral reef management and facilitate conservation strategies to mitigate coral bleaching worldwide
Published: 2020

25. The coral holobiont highlights the dependence of cnidarian animal hosts on their associated microbes

Author: Pogoreutz, C, Voolstra, CR, Rädecker, N, Weis, V, Cardenas, A, Raina, J-B, Pogoreutz, C, Voolstra, CR, Rädecker, N, Weis, V, Cardenas, A, and Raina, J-B
Published: 2020

26. Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment

Author: Camp EF, Suggett DJ, Pogoreutz C, Nitschke MR, Houlbreque F, Hume BCC, Gardner SG, Zampighi M, Rodolfo-Metalpa R, Voolstra CR, Camp EF, Suggett DJ, Pogoreutz C, Nitschke MR, Houlbreque F, Hume BCC, Gardner SG, Zampighi M, Rodolfo-Metalpa R, and Voolstra CR
Abstract: © 2020, Springer-Verlag GmbH Germany, part of Springer Nature. Climate change threatens the survival of scleractinian coral from exposure to concurrent ocean warming, acidification and deoxygenation; how corals can potentially adapt to this trio of stressors is currently unknown. This study investigates three coral species (Acropora muricata, Acropora pulchra and Porites lutea) dominant in an extreme mangrove lagoon (Bouraké, New Caledonia) where abiotic conditions exceed those predicted for many reef sites over the next 100 years under climate change and compared them to conspecifics from an environmentally more benign reef habitat. We studied holobiont physiology as well as plasticity in coral-associated microorganisms (Symbiodiniaceae and bacteria) through ITS2 and 16S rRNA sequencing, respectively. We hypothesised that differences in coral-associated microorganisms (Symbiodiniaceae and bacteria) between the lagoonal and adjacent reef habitats may support coral host productivity and ultimately the ability of corals to live in extreme environments. In the lagoon, all coral species exhibited a metabolic adjustment of reduced photosynthesis-to-respiration ratios (P/R), but this was accompanied by highly divergent coral host-specific microbial associations. This was substantiated by the absence of shared ITS2-type profiles (proxies for Symbiodiniaceae genotypes). We observed that ITS2 profiles originating from Durusdinium taxa made up < 3% and a novel Symbiodinium ITS2 profile A1-A1v associated with A. pulchra. Bacterial community profiles were also highly divergent in corals from the lagoonal environment, whereas corals from the reef site were consistently dominated by Hahellaceae, Endozoicomonas. As such, differences in host–microorganism associations aligned with different physiologies and habitats. Our results argue that a multitude of host–microorganism associations are required to fulfill the changing nutritional demands of corals persisting into environments t
Published: 2020

27. The coral holobiont highlights the dependence of cnidarian animal hosts on their associated microbes

Author: Pogoreutz, C, Voolstra, CR, Rädecker, N, Weis, V, Cardenas, A, Raina, J-B, Pogoreutz, C, Voolstra, CR, Rädecker, N, Weis, V, Cardenas, A, and Raina, J-B
Published: 2020

28. Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities

Author: Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME, Smith, DJ, Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME, and Smith, DJ
Abstract: © 2020 The Author(s). Background: The capacity of reef-building corals to tolerate (or adapt to) heat stress is a key factor determining their resilience to future climate change. Changes in coral microbiome composition (particularly for microalgal endosymbionts and bacteria) is a potential mechanism that may assist corals to thrive in warm waters. The northern Red Sea experiences extreme temperatures anomalies, yet corals in this area rarely bleach suggesting possible refugia to climate change. However, the coral microbiome composition, and how it relates to the capacity to thrive in warm waters in this region, is entirely unknown. Results: We investigated microbiomes for six coral species (Porites nodifera, Favia favus, Pocillopora damicornis, Seriatopora hystrix, Xenia umbellata, and Sarcophyton trocheliophorum) from five sites in the northern Red Sea spanning 4° of latitude and summer mean temperature ranges from 26.6 °C to 29.3 °C. A total of 19 distinct dinoflagellate endosymbionts were identified as belonging to three genera in the family Symbiodiniaceae (Symbiodinium, Cladocopium, and Durusdinium). Of these, 86% belonged to the genus Cladocopium, with notably five novel types (19%). The endosymbiont community showed a high degree of host-specificity despite the latitudinal gradient. In contrast, the diversity and composition of bacterial communities of the surface mucus layer (SML) - a compartment particularly sensitive to environmental change - varied significantly between sites, however for any given coral was species-specific. Conclusion: The conserved endosymbiotic community suggests high physiological plasticity to support holobiont productivity across the different latitudinal regimes. Further, the presence of five novel algal endosymbionts suggests selection of certain genotypes (or genetic adaptation) within the semi-isolated Red Sea. In contrast, the dynamic composition of bacteria associated with the SML across sites may contribute to holobiont fun
Published: 2020

29. Down to the bone: the role of overlooked endolithic microbiomes in reef coral health

Author: Pernice, M, Raina, JB, Rädecker, N, Cárdenas, A, Pogoreutz, C, Voolstra, CR, Pernice, M, Raina, JB, Rädecker, N, Cárdenas, A, Pogoreutz, C, and Voolstra, CR
Abstract: © 2019, The Author(s). Reef-building corals harbour an astonishing diversity of microorganisms, including endosymbiotic microalgae, bacteria, archaea, and fungi. The metabolic interactions within this symbiotic consortium are fundamental to the ecological success of corals and the unique productivity of coral reef ecosystems. Over the last two decades, scientific efforts have been primarily channelled into dissecting the symbioses occurring in coral tissues. Although easily accessible, this compartment is only 2–3 mm thick, whereas the underlying calcium carbonate skeleton occupies the vast internal volume of corals. Far from being devoid of life, the skeleton harbours a wide array of algae, endolithic fungi, heterotrophic bacteria, and other boring eukaryotes, often forming distinct bands visible to the bare eye. Some of the critical functions of these endolithic microorganisms in coral health, such as nutrient cycling and metabolite transfer, which could enable the survival of corals during thermal stress, have long been demonstrated. In addition, some of these microorganisms can dissolve calcium carbonate, weakening the coral skeleton and therefore may play a major role in reef erosion. Yet, experimental data are wanting due to methodological limitations. Recent technological and conceptual advances now allow us to tease apart the complex physical, ecological, and chemical interactions at the heart of coral endolithic microbial communities. These new capabilities have resulted in an excellent body of research and provide an exciting outlook to further address the functional microbial ecology of the “overlooked” coral skeleton.
Published: 2020

30. Erratum: Correction to: Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities (Microbiome (2020) 8 1 (8))

Author: Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME, Smith, DJ, Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME, and Smith, DJ
Abstract: Following publication of the original article [1], the authors reported an error on the legend of of P.damicornis in Fig. 1.
Published: 2020

31. Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities

Author: Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME, Smith, DJ, Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME, and Smith, DJ
Abstract: © 2020 The Author(s). Background: The capacity of reef-building corals to tolerate (or adapt to) heat stress is a key factor determining their resilience to future climate change. Changes in coral microbiome composition (particularly for microalgal endosymbionts and bacteria) is a potential mechanism that may assist corals to thrive in warm waters. The northern Red Sea experiences extreme temperatures anomalies, yet corals in this area rarely bleach suggesting possible refugia to climate change. However, the coral microbiome composition, and how it relates to the capacity to thrive in warm waters in this region, is entirely unknown. Results: We investigated microbiomes for six coral species (Porites nodifera, Favia favus, Pocillopora damicornis, Seriatopora hystrix, Xenia umbellata, and Sarcophyton trocheliophorum) from five sites in the northern Red Sea spanning 4° of latitude and summer mean temperature ranges from 26.6 °C to 29.3 °C. A total of 19 distinct dinoflagellate endosymbionts were identified as belonging to three genera in the family Symbiodiniaceae (Symbiodinium, Cladocopium, and Durusdinium). Of these, 86% belonged to the genus Cladocopium, with notably five novel types (19%). The endosymbiont community showed a high degree of host-specificity despite the latitudinal gradient. In contrast, the diversity and composition of bacterial communities of the surface mucus layer (SML) - a compartment particularly sensitive to environmental change - varied significantly between sites, however for any given coral was species-specific. Conclusion: The conserved endosymbiotic community suggests high physiological plasticity to support holobiont productivity across the different latitudinal regimes. Further, the presence of five novel algal endosymbionts suggests selection of certain genotypes (or genetic adaptation) within the semi-isolated Red Sea. In contrast, the dynamic composition of bacteria associated with the SML across sites may contribute to holobiont fun
Published: 2020

32. Down to the bone: the role of overlooked endolithic microbiomes in reef coral health

Author: Pernice, M, Raina, JB, Rädecker, N, Cárdenas, A, Pogoreutz, C, Voolstra, CR, Pernice, M, Raina, JB, Rädecker, N, Cárdenas, A, Pogoreutz, C, and Voolstra, CR
Abstract: © 2019, The Author(s). Reef-building corals harbour an astonishing diversity of microorganisms, including endosymbiotic microalgae, bacteria, archaea, and fungi. The metabolic interactions within this symbiotic consortium are fundamental to the ecological success of corals and the unique productivity of coral reef ecosystems. Over the last two decades, scientific efforts have been primarily channelled into dissecting the symbioses occurring in coral tissues. Although easily accessible, this compartment is only 2–3 mm thick, whereas the underlying calcium carbonate skeleton occupies the vast internal volume of corals. Far from being devoid of life, the skeleton harbours a wide array of algae, endolithic fungi, heterotrophic bacteria, and other boring eukaryotes, often forming distinct bands visible to the bare eye. Some of the critical functions of these endolithic microorganisms in coral health, such as nutrient cycling and metabolite transfer, which could enable the survival of corals during thermal stress, have long been demonstrated. In addition, some of these microorganisms can dissolve calcium carbonate, weakening the coral skeleton and therefore may play a major role in reef erosion. Yet, experimental data are wanting due to methodological limitations. Recent technological and conceptual advances now allow us to tease apart the complex physical, ecological, and chemical interactions at the heart of coral endolithic microbial communities. These new capabilities have resulted in an excellent body of research and provide an exciting outlook to further address the functional microbial ecology of the “overlooked” coral skeleton.
Published: 2020

33. Coral microbiome diversity reflects mass coral bleaching susceptibility during the 2016 El Niño heat wave

Author: Gardner, SG, Camp, EF, Smith, DJ, Kahlke, T, Osman, EO, Gendron, G, Hume, BCC, Pogoreutz, C, Voolstra, CR, Suggett, DJ, Gardner, SG, Camp, EF, Smith, DJ, Kahlke, T, Osman, EO, Gendron, G, Hume, BCC, Pogoreutz, C, Voolstra, CR, and Suggett, DJ
Abstract: Repeat marine heat wave-induced mass coral bleaching has decimated reefs in Seychelles for 35 years, but how coral-associated microbial diversity (microalgal endosymbionts of the family Symbiodiniaceae and bacterial communities) potentially underpins broad-scale bleaching dynamics remains unknown. We assessed microbiome composition during the 2016 heat wave peak at two contrasting reef sites (clear vs. turbid) in Seychelles, for key coral species considered bleaching sensitive (Acropora muricata, Acropora gemmifera) or tolerant (Porites lutea, Coelastrea aspera). For all species and sites, we sampled bleached versus unbleached colonies to examine how microbiomes align with heat stress susceptibility. Over 30% of all corals bleached in 2016, half of which were from Acropora sp. and Pocillopora sp. mass bleaching that largely transitioned to mortality by 2017. Symbiodiniaceae ITS2-sequencing revealed that the two Acropora sp. and P. lutea generally associated with C3z/C3 and C15 types, respectively, whereas C. aspera exhibited a plastic association with multiple D types and two C3z types. 16S rRNA gene sequencing revealed that bacterial communities were coral host-specific, largely through differences in the most abundant families, Hahellaceae (comprising Endozoicomonas), Rhodospirillaceae, and Rhodobacteraceae. Both Acropora sp. exhibited lower bacterial diversity, species richness, and community evenness compared to more bleaching-resistant P. lutea and C. aspera. Different bleaching susceptibility among coral species was thus consistent with distinct microbiome community profiles. These profiles were conserved across bleached and unbleached colonies of all coral species. As this pattern could also reflect a parallel response of the microbiome to environmental changes, the detailed functional associations will need to be determined in future studies. Further understanding such microbiome-environmental interactions is likely critical to target more effective manageme
Published: 2019

34. Large expert-curated database for benchmarking document similarity detection in biomedical literature search

Author: Brown, P, Tan, A-C, El-Esawi, MA, Liehr, T, Blanck, O, Gladue, DP, Almeida, GMF, Cernava, T, Sorzano, CO, Yeung, AWK, Engel, MS, Chandrasekaran, AR, Muth, T, Staege, MS, Daulatabad, SV, Widera, D, Zhang, J, Meule, A, Honjo, K, Pourret, O, Yin, C-C, Zhang, Z, Cascella, M, Flegel, WA, Goodyear, CS, van Raaij, MJ, Bukowy-Bieryllo, Z, Campana, LG, Kurniawan, NA, Lalaouna, D, Huttner, FJ, Ammerman, BA, Ehret, F, Cobine, PA, Tan, E-C, Han, H, Xia, W, McCrum, C, Dings, RPM, Marinello, F, Nilsson, H, Nixon, B, Voskarides, K, Yang, L, Costa, VD, Bengtsson-Palme, J, Bradshaw, W, Grimm, DG, Kumar, N, Martis, E, Prieto, D, Sabnis, SC, Amer, SEDR, Liew, AWC, Perco, P, Rahimi, F, Riva, G, Zhang, C, Devkota, HP, Ogami, K, Basharat, Z, Fierz, W, Siebers, R, Tan, K-H, Boehme, KA, Brenneisen, P, Brown, JAL, Dalrymple, BP, Harvey, DJ, Ng, G, Werten, S, Bleackley, M, Dai, Z, Dhariwal, R, Gelfer, Y, Hartmann, MD, Miotla, P, Tamaian, R, Govender, P, Gurney-Champion, OJ, Kauppila, JH, Zhang, X, Echeverria, N, Subhash, S, Sallmon, H, Tofani, M, Bae, T, Bosch, O, Cuiv, PO, Danchin, A, Diouf, B, Eerola, T, Evangelou, E, Filipp, FV, Klump, H, Kurgan, L, Smith, SS, Terrier, O, Tuttle, N, Ascher, DB, Janga, SC, Schulte, LN, Becker, D, Browngardt, C, Bush, SJ, Gaullier, G, Ide, K, Meseko, C, Werner, GDA, Zaucha, J, Al-Farha, AA, Greenwald, NF, Popoola, SI, Rahman, MS, Xu, J, Yang, SY, Hiroi, N, Alper, OM, Baker, CI, Bitzer, M, Chacko, G, Debrabant, B, Dixon, R, Forano, E, Gilliham, M, Kelly, S, Klempnauer, K-H, Lidbury, BA, Lin, MZ, Lynch, I, Ma, W, Maibach, EW, Mather, DE, Nandakumar, KS, Ohgami, RS, Parchi, P, Tressoldi, P, Xue, Y, Armitage, C, Barraud, P, Chatzitheochari, S, Coelho, LP, Diao, J, Doxey, AC, Gobet, A, Hu, P, Kaiser, S, Mitchell, KM, Salama, MF, Shabalin, IG, Song, H, Stevanovic, D, Yadollahpour, A, Zeng, E, Zinke, K, Alimba, CG, Beyene, TJ, Cao, Z, Chan, SS, Gatchell, M, Kleppe, A, Piotrowski, M, Torga, G, Woldesemayat, AA, Cosacak, MI, Haston, S, Ross, SA, Williams, R, Wong, A, Abramowitz, MK, Effiong, A, Lee, S, Abid, MB, Agarabi, C, Alaux, C, Albrecht, DR, Atkins, GJ, Beck, CR, Bonvin, AMJJ, Bourke, E, Brand, T, Braun, RJ, Bull, JA, Cardoso, P, Carter, D, Delahay, RM, Ducommun, B, Duijf, PHG, Epp, T, Eskelinen, E-L, Fallah, M, Farber, DB, Fernandez-Triana, J, Feyerabend, F, Florio, T, Friebe, M, Furuta, S, Gabrielsen, M, Gruber, J, Grybos, M, Han, Q, Heinrich, M, Helantera, H, Huber, M, Jeltsch, A, Jiang, F, Josse, C, Jurman, G, Kamiya, H, de Keersmaecker, K, Kristiansson, E, de Leeuw, F-E, Li, J, Liang, S, Lopez-Escamez, JA, Lopez-Ruiz, FJ, Marchbank, KJ, Marschalek, R, Martin, CS, Miele, AE, Montagutelli, X, Morcillo, E, Nicoletti, R, Niehof, M, O'Toole, R, Ohtomo, T, Oster, H, Palma, J-A, Paterson, R, Peifer, M, Portilla, M, Portillo, MC, Pritchard, AL, Pusch, S, Raghava, GPS, Roberts, NJ, Ross, K, Schuele, B, Sergeant, K, Shen, J, Stella, A, Sukocheva, O, Uversky, VN, Vanneste, S, Villet, MH, Viveiros, M, Vorholt, JA, Weinstock, C, 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and Zhou, Y
Published: 2019

35. Large expert-curated database for benchmarking document similarity detection in biomedical literature search

Author: Brown, P, Tan, A-C, El-Esawi, MA, Liehr, T, Blanck, O, Gladue, DP, Almeida, GMF, Cernava, T, Sorzano, CO, Yeung, AWK, Engel, MS, Chandrasekaran, AR, Muth, T, Staege, MS, Daulatabad, SV, Widera, D, Zhang, J, Meule, A, Honjo, K, Pourret, O, Yin, C-C, Zhang, Z, Cascella, M, Flegel, WA, Goodyear, CS, van Raaij, MJ, Bukowy-Bieryllo, Z, Campana, LG, Kurniawan, NA, Lalaouna, D, Huttner, FJ, Ammerman, BA, Ehret, F, Cobine, PA, Tan, E-C, Han, H, Xia, W, McCrum, C, Dings, RPM, Marinello, F, Nilsson, H, Nixon, B, Voskarides, K, Yang, L, Costa, VD, Bengtsson-Palme, J, Bradshaw, W, Grimm, DG, Kumar, N, Martis, E, Prieto, D, Sabnis, SC, Amer, SEDR, Liew, AWC, Perco, P, Rahimi, F, Riva, G, Zhang, C, Devkota, HP, Ogami, K, Basharat, Z, Fierz, W, Siebers, R, Tan, K-H, Boehme, KA, Brenneisen, P, Brown, JAL, Dalrymple, BP, Harvey, DJ, Ng, G, Werten, S, Bleackley, M, Dai, Z, Dhariwal, R, Gelfer, Y, Hartmann, MD, Miotla, P, Tamaian, R, Govender, P, Gurney-Champion, OJ, Kauppila, JH, Zhang, X, 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A, Gao, T, Asefa, NG, Giganti, F, Grabowski, P, Guerra-Mora, JR, Guo, C, Guo, X, Gupta, H, He, S, Heijne, M, Heinemann, S, Hogrebe, A, Huang, Z, Iskander-Rizk, S, Iyer, LM, Jahan, Y, James, AS, Joel, E, Joffroy, B, Jegousse, C, Kambondo, G, Karnati, P, Kaya, C, Ke, A, Kelly, D, Kickert, R, Kidibule, PE, Kieselmann, JP, Kim, HJ, Kitazawa, T, Lamberts, A, Liang, H, Linn, SN, Litfin, T, Liusuo, W, Lygirou, V, Mahato, AK, Mai, Z-M, Major, RW, Mali, S, Mallis, P, Mao, W, Marvin-Dowle, K, Mason, LD, Merideth, B, Merino-Plaza, MJ, Merlaen, B, Messina, R, Mishra, AK, Muhammad, J, Musinguzi, C, Nanou, A, Naqash, A, Nguyen, JT, Nguyen, TTH, Ni, D, Nida, Notcovich, S, Ohst, B, Ollivier, QR, Osses, DF, Peng, X, Plantinga, A, Pulia, M, Rafiq, M, Raman, A, Raucher-Chene, D, Rawski, R, Ray, A, Razak, LA, Rudolf, K, Rusch, P, Sadoine, ML, Schmidt, A, Schurr, R, Searles, S, Sharma, S, Sheehan, B, Shi, C, Shohayeb, B, Sommerlad, A, Strehlow, J, Sun, X, Sundar, R, Taherzadeh, G, Tahir, NDM, Tang, J, 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G, Lewis, JS, Kanj, SS, Kaur, H, Kheir, F, Kichatova, VS, Kiyani, M, Klein, R, Kovesi, T, Kraschnewski, JL, Kumar, AP, Labutin, D, Lazo-Langner, A, Leclercq, G, Li, M, Li, Q, Li, T, Liao, W-T, Liao, Z-Y, Lin, J, Lizer, J, Lobreglio, G, Lowies, C, Lu, C, Majeed, H, Martin, A, Martinez-Sobrido, L, Meresh, E, Middelveen, M, Mohebbi, A, Mota, J, Mozaheb, Z, Muyaya, L, Nandhakumar, A, Ng, SHX, Obeidat, M, Oh, D-H, Owais, M, Pace-Asciak, P, Panwar, A, Patterson, C, Penagos-Tabaree, F, Pianosi, PT, Pinzi, V, Pridans, C, Psaroulaki, A, Pujala, RK, Pulido-Arjona, L, Qi, P-F, Rahman, P, Rai, NK, Rassaf, T, Refardt, J, Ricciardi, W, Riess, O, Rovas, A, Sacks, FM, Saleh, S, Sampson, C, Schmutz, A, Sepanski, R, Sharma, N, Spearman, P, Subramaniapillai, M, Swali, R, Tan, CM, Tellechea, JI, Thomas, L-M, Tong, X, Veys, R, Vitriol, V, Wang, H-D, Waugh, J, Webb, SA, Williams, BA, Workman, AD, Xiang, T, Xie, L-X, Xu, T, Yang, C, Yoon, JG, Yuan, CM, Zaritsky, A, Zhao, H, Zuckerman, H, Lyu, R, Pullan, W, and Zhou, Y
Published: 2019

36. Corals of the Red Sea

Author: Voolstra, CR, Berumen, ML, Berumen, M, Arrigoni, R, Bouwmeester, J, Terraneo, T, Benzoni, F, Berumen ML, Arrigoni R, Bouwmeester J, Terraneo TI, Benzoni F, Voolstra, CR, Berumen, ML, Berumen, M, Arrigoni, R, Bouwmeester, J, Terraneo, T, Benzoni, F, Berumen ML, Arrigoni R, Bouwmeester J, Terraneo TI, and Benzoni F
Abstract: The biodiversity of Red Sea corals captured the attention of some of the earliest European natural historians. Many of the first descriptions of tropical reef corals were based on Red Sea material. Modern approaches to resolve the notorious challenges of coral taxonomy have only recently been applied to Red Sea taxa. This chapter reviews current knowledge of the distributions of coral species in the Arabian region, including assessments of endemism. We also review new species described (or resurrected) since the last major assessment (in 2002). Where sufficient data is available, we highlight within-region distribution patterns. The Red Sea has the highest levels of endemism among all regions of the Indian Ocean. Analysis of the similarity of species composition among the Arabian subregions shows that the Red Sea and Socotra Island are the most speciose, but also have distinct community compositions. The regional diversity of Red Sea corals is likely influenced by the unique environmental gradients of the Arabian region. Despite evolving in testing conditions, Red Sea corals have been impacted by global climate change. Recent thermal bleaching events in the Red Sea highlight the pressures and challenges to future recovery.
Published: 2019

37. Coral microbiome diversity reflects mass coral bleaching susceptibility during the 2016 El Niño heat wave

Author: Gardner, SG, Camp, EF, Smith, DJ, Kahlke, T, Osman, EO, Gendron, G, Hume, BCC, Pogoreutz, C, Voolstra, CR, Suggett, DJ, Gardner, SG, Camp, EF, Smith, DJ, Kahlke, T, Osman, EO, Gendron, G, Hume, BCC, Pogoreutz, C, Voolstra, CR, and Suggett, DJ
Abstract: © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Repeat marine heat wave-induced mass coral bleaching has decimated reefs in Seychelles for 35 years, but how coral-associated microbial diversity (microalgal endosymbionts of the family Symbiodiniaceae and bacterial communities) potentially underpins broad-scale bleaching dynamics remains unknown. We assessed microbiome composition during the 2016 heat wave peak at two contrasting reef sites (clear vs. turbid) in Seychelles, for key coral species considered bleaching sensitive (Acropora muricata, Acropora gemmifera) or tolerant (Porites lutea, Coelastrea aspera). For all species and sites, we sampled bleached versus unbleached colonies to examine how microbiomes align with heat stress susceptibility. Over 30% of all corals bleached in 2016, half of which were from Acropora sp. and Pocillopora sp. mass bleaching that largely transitioned to mortality by 2017. Symbiodiniaceae ITS2-sequencing revealed that the two Acropora sp. and P. lutea generally associated with C3z/C3 and C15 types, respectively, whereas C. aspera exhibited a plastic association with multiple D types and two C3z types. 16S rRNA gene sequencing revealed that bacterial communities were coral host-specific, largely through differences in the most abundant families, Hahellaceae (comprising Endozoicomonas), Rhodospirillaceae, and Rhodobacteraceae. Both Acropora sp. exhibited lower bacterial diversity, species richness, and community evenness compared to more bleaching-resistant P. lutea and C. aspera. Different bleaching susceptibility among coral species was thus consistent with distinct microbiome community profiles. These profiles were conserved across bleached and unbleached colonies of all coral species. As this pattern could also reflect a parallel response of the microbiome to environmental changes, the detailed functional associations will need to be determined in future studies. Further understanding such microbiome-e
Published: 2019

38. Molecular techniques and their limitations shape our view of the holobiont

Author: Cooke, I, Mead, O, Whalen, C, Boote, C, Moya, A, Ying, H, Robbins, S, Strugnell, JM, Darling, A, Miller, D, Voolstra, CR, Adamska, M, Cooke, I, Mead, O, Whalen, C, Boote, C, Moya, A, Ying, H, Robbins, S, Strugnell, JM, Darling, A, Miller, D, Voolstra, CR, and Adamska, M
Abstract: © 2019 Elsevier GmbH It is now recognised that the biology of almost any organism cannot be fully understood without recognising the existence and potential functional importance of associated microbes. Arguably, the emergence of this holistic viewpoint may never have occurred without the development of a crucial molecular technique, 16S rDNA amplicon sequencing, which allowed microbial communities to be easily profiled across a broad range of contexts. A diverse array of molecular techniques are now used to profile microbial communities, infer their evolutionary histories, visualise them in host tissues, and measure their molecular activity. In this review, we examine each of these categories of measurement and inference with a focus on the questions they make tractable, and the degree to which their capabilities and limitations shape our view of the holobiont.
Published: 2019

39. Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches

Author: Jaspers, C, Fraune, S, Arnold, AE, Miller, DJ, Bosch, TCG, Voolstra, CR, Jaspers, C, Fraune, S, Arnold, AE, Miller, DJ, Bosch, TCG, and Voolstra, CR
Published: 2019

40. Large expert-curated database for benchmarking document similarity detection in biomedical literature search

Author: Brown, P, Tan, A-C, El-Esawi, MA, Liehr, T, Blanck, O, Gladue, DP, Almeida, GMF, Cernava, T, Sorzano, CO, Yeung, AWK, Engel, MS, Chandrasekaran, AR, Muth, T, Staege, MS, Daulatabad, SV, Widera, D, Zhang, J, Meule, A, Honjo, K, Pourret, O, Yin, C-C, Zhang, Z, Cascella, M, Flegel, WA, Goodyear, CS, van Raaij, MJ, Bukowy-Bieryllo, Z, Campana, LG, Kurniawan, NA, Lalaouna, D, Huttner, FJ, Ammerman, BA, Ehret, F, Cobine, PA, Tan, E-C, Han, H, Xia, W, McCrum, C, Dings, RPM, Marinello, F, Nilsson, H, Nixon, B, Voskarides, K, Yang, L, Costa, VD, Bengtsson-Palme, J, Bradshaw, W, Grimm, DG, Kumar, N, Martis, E, Prieto, D, Sabnis, SC, Amer, SEDR, Liew, AWC, Perco, P, Rahimi, F, Riva, G, Zhang, C, Devkota, HP, Ogami, K, Basharat, Z, Fierz, W, Siebers, R, Tan, K-H, Boehme, KA, Brenneisen, P, Brown, JAL, Dalrymple, BP, Harvey, DJ, Ng, G, Werten, S, Bleackley, M, Dai, Z, Dhariwal, R, Gelfer, Y, Hartmann, MD, Miotla, P, Tamaian, R, Govender, P, Gurney-Champion, OJ, Kauppila, JH, Zhang, X, Echeverria, N, Subhash, S, Sallmon, H, Tofani, M, Bae, T, Bosch, O, Cuiv, PO, Danchin, A, Diouf, B, Eerola, T, Evangelou, E, Filipp, FV, Klump, H, Kurgan, L, Smith, SS, Terrier, O, Tuttle, N, Ascher, DB, Janga, SC, Schulte, LN, Becker, D, Browngardt, C, Bush, SJ, Gaullier, G, Ide, K, Meseko, C, Werner, GDA, Zaucha, J, Al-Farha, AA, Greenwald, NF, Popoola, SI, Rahman, MS, Xu, J, Yang, SY, Hiroi, N, Alper, OM, Baker, CI, Bitzer, M, Chacko, G, Debrabant, B, Dixon, R, Forano, E, Gilliham, M, Kelly, S, Klempnauer, K-H, Lidbury, BA, Lin, MZ, Lynch, I, Ma, W, Maibach, EW, Mather, DE, Nandakumar, KS, Ohgami, RS, Parchi, P, Tressoldi, P, Xue, Y, Armitage, C, Barraud, P, Chatzitheochari, S, Coelho, LP, Diao, J, Doxey, AC, Gobet, A, Hu, P, Kaiser, S, Mitchell, KM, Salama, MF, Shabalin, IG, Song, H, Stevanovic, D, Yadollahpour, A, Zeng, E, Zinke, K, Alimba, CG, Beyene, TJ, Cao, Z, Chan, SS, Gatchell, M, Kleppe, A, Piotrowski, M, Torga, G, Woldesemayat, AA, Cosacak, MI, Haston, S, Ross, SA, Williams, R, Wong, A, Abramowitz, MK, Effiong, A, Lee, S, Abid, MB, Agarabi, C, Alaux, C, Albrecht, DR, Atkins, GJ, Beck, CR, Bonvin, AMJJ, Bourke, E, Brand, T, Braun, RJ, Bull, JA, Cardoso, P, Carter, D, Delahay, RM, Ducommun, B, Duijf, PHG, Epp, T, Eskelinen, E-L, Fallah, M, Farber, DB, Fernandez-Triana, J, Feyerabend, F, Florio, T, Friebe, M, Furuta, S, Gabrielsen, M, Gruber, J, Grybos, M, Han, Q, Heinrich, M, Helantera, H, Huber, M, Jeltsch, A, Jiang, F, Josse, C, Jurman, G, Kamiya, H, de Keersmaecker, K, Kristiansson, E, de Leeuw, F-E, Li, J, Liang, S, Lopez-Escamez, JA, Lopez-Ruiz, FJ, Marchbank, KJ, Marschalek, R, Martin, CS, Miele, AE, Montagutelli, X, Morcillo, E, Nicoletti, R, Niehof, M, O'Toole, R, Ohtomo, T, Oster, H, Palma, J-A, Paterson, R, Peifer, M, Portilla, M, Portillo, MC, Pritchard, AL, Pusch, S, Raghava, GPS, Roberts, NJ, Ross, K, Schuele, B, Sergeant, K, Shen, J, Stella, A, Sukocheva, O, Uversky, VN, Vanneste, S, Villet, MH, Viveiros, M, Vorholt, JA, Weinstock, C, Yamato, M, Zabetakis, I, Zhao, X, Ziegler, A, Aizat, WM, Atlas, L, Bridges, KM, Chakraborty, S, Deschodt, M, Domingues, HS, Esfahlani, SS, Falk, S, Guisado, JL, Kane, NC, Kueberuwa, G, Lau, CL, Liang, D, Liu, E, Luu, AM, Ma, C, Ma, L, Moyer, R, Norris, AD, Panthee, S, Parsons, JR, Peng, Y, Pinto, IM, Reschke, CR, Sillanpaa, E, Stewart, CJ, Uhle, F, Yang, H, Zhou, K, Zhu, S, Ashry, M, Bergsland, N, Berthold, M, Chen, C-E, Colella, V, Cuypers, M, Eskew, EA, Fan, X, Gajda, M, Gonzalezlez-Prendes, R, Goodin, A, Graham, EB, Groen, EJN, Gutierrez-Sacristan, A, Habes, M, Heffler, E, Higginbottom, DB, Janzen, T, Jayaraman, J, Jibb, LA, Jongen, S, Kinyanjui, T, Koleva-Kolarova, RG, Li, Z, Liu, Y-P, Lund, BA, Lussier, AA, Mier, P, Moore, MD, Nagler, K, Orme, MW, Pearson, JA, Prajapati, AS, Saito, Y, Troder, SE, Uchendu, F, Verloh, N, Voutchkova, DD, Abu-Zaid, A, Bakkach, J, Baumert, P, Dono, M, Hanson, J, Herbelet, S, Hobbs, E, Kulkarni, A, Liu, S, Loft, ND, Reddan, T, Senghore, T, Vindin, H, Xu, H, Bannon, R, Chen, B, Cheung, JTK, Cooper, J, Esnakul, AK, Feghali, KA, Ghelardi, E, Gnasso, A, Horbar, J, Lai, HM, Ma, R, Pan, Z, Peres, MA, Pranata, R, Seow, E, Sydes, M, Testoni, I, Westermair, AL, Yang, Y, Afnan, M, Albiol, J, Albuquerque, LG, Amiya, E, Amorim, RM, An, Q, Andersen, SU, Aplin, JD, Argyropoulos, C, Asmann, YW, Assaeed, AM, Atanasov, AG, Atchison, DA, Avery, SV, Avillach, P, Baade, PD, Backman, L, Badie, C, Baldi, A, Ball, E, Bardot, O, Barnett, AG, Basner, M, Batra, J, Bazanova, OM, Beale, A, Beddoe, T, Bell, ML, Berezikov, E, Berners-Price, S, Bernhardt, P, Berry, E, Bessa, TB, Billington, C, Birch, J, Blakely, RD, Blaskovich, MAT, Blum, R, Boelaert, M, Bogdanos, D, Bosch, C, Bourgoin, T, Bouvard, D, Boykin, LM, Bradley, G, Braun, D, Brownlie, J, Bruhl, A, Burt, A, Butler, LM, Byrareddy, SN, Byrne, HJ, Cabantous, S, Calatayud, S, Candal, E, Carlson, K, Casillas, S, Castelvetro, V, Caswell, PT, Cavalli, G, Cerovsky, V, Chagoyen, M, Chen, C-S, Chen, DF, Chen, H, Chen, J-T, Chen, Y, Cheng, C, Cheng, J, Chinapaw, M, Chinopoulos, C, Cho, WCS, Chong, L, Chowdhury, D, Chwalibog, A, Ciresi, A, Cockcroft, S, Conesa, A, Cook, PA, Cooper, DN, Coqueret, O, Corea, EM, Costa, E, Coupland, C, Crawford, SY, Cruz, AD, Cui, H, Cui, Q, Culver, DC, D'Angiulli, A, Dahms, TES, Daigle, F, Dalgleish, R, Danielsen, HE, Darras, S, Davidson, SM, Day, DA, Degirmenci, V, Demaison, L, Devriendt, K, Ding, J, Dogan, Y, Dong, XC, Donner, CF, Dressick, W, Drevon, CA, Duan, H, Ducho, C, Dumaz, N, Dwarakanath, BS, Ebell, MH, Eisenhardt, S, Elkum, N, Engel, N, Erickson, TB, Fairhead, M, Faville, MJ, Fejzo, MS, Festa, F, Feteira, A, Flood-Page, P, Forsayeth, J, Fox, SA, Franks, SJ, Frentiu, FD, Frilander, MJ, Fu, X, Fujita, S, Galea, I, Galluzzi, L, Gani, F, Ganpule, AP, Garcia-Alix, A, Gedye, K, Giordano, M, Giunta, C, Gleeson, PA, Goarant, C, Gong, H, Gora, D, Gough, MJ, Goyal, R, Graham, KE, Grande-Perez, A, Graves, PM, Greidanus, H, Grice, D, Grunau, C, Gumulya, Y, Guo, Y, Gurevich, VV, Gusev, O, Hacker, E, Hage, SR, Hagen, G, Hahn, S, Haller, DM, Hammerschmidt, S, Han, J, Han, R, Handfield, M, Hapuarachchi, HC, Harder, T, Hardingham, JE, Heck, M, Heers, M, Hew, KF, Higuchi, Y, St Hilaire, C, Hilton, R, Hodzic, E, Hone, A, Hongoh, Y, Hu, G, Huber, HP, Hueso, LE, Huirne, J, Hurt, L, Idborg, H, Ikeo, K, Ingley, E, Jakeman, PM, Jensen, A, Jia, H, Jia, S, Jiang, J, Jiang, X, Jin, Y, Jo, D, Johnson, AM, Johnston, M, Jonscher, KR, Jorens, PG, Jorgensen, JOL, Joubert, JW, Jung, S-H, Junior, AM, Kahan, T, Kamboj, SK, Kang, Y-K, Karamanos, Y, Karp, NA, Kelly, R, Kenna, R, Kennedy, J, Kersten, B, Khalaf, RA, Khalid, JM, Khatlani, T, Khider, T, Kijanka, GS, King, SRB, Kluz, T, Knox, P, Kobayashi, T, Koch, K-W, Kohonen-Corish, MRJ, Kong, X, Konkle-Parker, D, Korpela, KM, Kostrikis, LG, Kraiczy, P, Kratz, H, Krause, G, Krebsbach, PH, Kristensen, SR, Kumari, P, Kunimatsu, A, Kurdak, H, Kwon, YD, Lachat, C, Lagisz, M, Laky, B, Lammerding, J, Lange, M, Larrosa, M, Laslett, AL, LeClair, EE, Lee, K-W, Lee, M-Y, Lee, M-S, Li, G, Lieb, K, Lim, YY, Lindsey, ML, Line, P-D, Liu, D, Liu, F, Liu, H, Lloyd, VK, Lo, T-W, Locci, E, Loidl, J, Lorenzen, J, Lorkowski, S, Lovell, NH, Lu, H, Lu, W, Lu, Z, Luengo, GS, Lundh, L-G, Lysy, PA, Mabb, A, Mack, HG, Mackey, DA, Mahdavi, SR, Maher, P, Maher, T, Maity, SN, Malgrange, B, Mamoulakis, C, Mangoni, AA, Manke, T, Manstead, ASR, Mantalaris, A, Marsal, J, Marschall, H-U, Martin, FL, Martinez-Raga, J, Martinez-Salas, E, Mathieu, D, Matsui, Y, Maza, E, McCutcheon, JE, Mckay, GJ, McMillan, B, McMillan, N, Meads, C, Medina, L, Merrick, BA, Metzger, DW, Meunier, FA, Michaelis, M, Micheau, O, Mihara, H, Mintz, EM, Mizukami, T, Moalic, Y, Mohapatra, DP, Monteiro, A, Montes, M, Moran, JV, Morozov, SY, Mort, M, Murai, N, Murphy, DJ, Murphy, SK, Murray, SA, Naganawa, S, Nammi, S, Nasios, G, Natoli, RM, Nguyen, F, Nicol, C, van Nieuwerburgh, F, Nilsen, EB, Nobile, CJ, O'Mahony, M, Ohlsson, S, Olatunbosun, O, Olofsson, P, Ortiz, A, Ostrikov, K, Otto, S, Outeiro, TF, Ouyang, S, Paganoni, S, Page, A, Palm, C, Paradies, Y, Parsons, MH, Parsons, N, Pascal, P, Paul, E, Peckham, M, Pedemonte, N, Pellizzon, MA, Petrelli, M, Pichugin, A, Pinto, CJC, Plevris, JN, Pollesello, P, Polz, M, Ponti, G, Porcelli, P, Prince, M, Quinn, GP, Quinn, TJ, Ramula, S, Rappsilber, J, Rehfeldt, F, Reiling, JH, Remacle, C, Rezaei, M, Riddick, EW, Ritter, U, Roach, NW, Roberts, DD, Robles, G, Rodrigues, T, Rodriguez, C, Roislien, J, Roobol, MJ, Rowe, JA, Ruepp, A, van Ruitenbeek, J, Rust, P, Saad, S, Sack, GH, Santos, M, Saudemont, A, Sava, G, Schrading, S, Schramm, A, Schreiber, M, Schuler, S, Schymkowitz, J, Sczyrba, A, Seib, KL, Shi, H-P, Shimada, T, Shin, J-S, Shortt, C, Silveyra, P, Skinner, D, Small, I, Smeets, PAM, So, P-W, Solano, F, Sonenshine, DE, Song, J, Southall, T, Speakman, JR, Srinivasan, MV, Stabile, LP, Stasiak, A, Steadman, KJ, Stein, N, Stephens, AW, Stewart, DI, Stine, K, Storlazzi, C, Stoynova, NV, Strzalka, W, Suarez, OM, Sultana, T, Sumant, AV, Summers, MJ, Sun, G, Tacon, P, Tanaka, K, Tang, H, Tanino, Y, Targett-Adams, P, Tayebi, M, Tayyem, R, Tebbe, CC, Telfer, EE, Tempel, W, Teodorczyk-Injeyan, JA, Thijs, G, Thorne, S, Thrift, AG, Tiffon, C, Tinnefeld, P, Tjahjono, DH, Tolle, F, Toth, E, del Tredici, AL, Tsapas, A, Tsirigotis, K, Turak, A, Tzotzos, G, Udo, EE, Utsumi, T, Vaidyanathan, S, Vaillant, M, Valsesia, A, Vandenbroucke, RE, Veiga, FH, Vendrell, M, Vesk, PA, Vickers, P, Victor, VM, Villemur, R, Vohl, M-C, Voolstra, CR, Vuillemin, A, Wakelin, S, Waldron, L, Walsh, LJ, Wang, AY, Wang, F, Wang, Y, Watanabe, Y, Weigert, A, Wen, J-C, Wham, C, White, EP, Wiener, J, Wilharm, G, Wilkinson, S, Willmann, R, Wilson, C, Wirth, B, Wojan, TR, Wolff, M, Wong, BM, Wu, T-W, Wuerbel, H, Xiao, X, Xu, D, Xu, JW, Xue, B, Yalcin, S, Yan, H, Yang, E-C, Yang, S, Yang, W, Ye, Y, Ye, Z-Q, Yli-Kauhaluoma, J, Yoneyama, H, Yu, Y, Yuan, G-C, Yuh, C-H, Zaccolo, M, Zeng, C, Zevnik, B, Zhang, L, Zhang, Y, 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Strobl, F, Subissi, L, Supriyanto, I, Surve, CR, Suzuki, T, Syme, C, Sorelius, K, Tang, Y, Tantawy, M, Tennakoon, S, Teseo, S, Toelzer, C, Tomov, N, Tovar, M, Tran, L, Tripathi, S, Tuladhar, AM, Ukubuiwe, AC, Ung, COL, Valgepea, K, Vatanparast, H, Vidal, A, Wang, Q, Watari, R, Webster, R, Wei, J, Wibowo, D, Wingenbach, TSH, Xavier, RM, Xiao, S, Xiong, P, Xu, S, Yao, R, Yao, W, Yin, Q, Zaitsu, M, Zeineb, Z, Zhan, X-Y, Zhang, R, Zhang, W, Zheng, S, Zhou, B, Ahmad, H, Akinwumi, SA, Albery, GF, Alhowimel, A, Ali, J, Alshehri, M, Alsuhaibani, M, Anikin, A, Azubuike, SO, Bach-Mortensen, A, Baltiansky, L, Bartas, M, Belachew, KY, Bhardwaj, V, Binder, K, Bland, NS, Boah, M, Bullen, B, Calabro, GE, Callahan, TJ, Cao, B, Chalmers, K, Chang, W, Che, Z, Chen, ATY, Chen, Z, Choi, Y, Chowdhury, MAK, Christensen, MR, Cooke, RSC, Cottini, M, Covington, NV, Cunningham, C, Delarocque, J, Devos, L, Dhar, AR, Ding, K-F, Dong, K, Dong, Z, Dreyer, N, Ekstrand, C, Fardet, T, Feleke, BE, Feurer, T, Freitas, A, Gao, T, Asefa, NG, Giganti, F, Grabowski, P, Guerra-Mora, JR, Guo, C, Guo, X, Gupta, H, He, S, Heijne, M, Heinemann, S, Hogrebe, A, Huang, Z, Iskander-Rizk, S, Iyer, LM, Jahan, Y, James, AS, Joel, E, Joffroy, B, Jegousse, C, Kambondo, G, Karnati, P, Kaya, C, Ke, A, Kelly, D, Kickert, R, Kidibule, PE, Kieselmann, JP, Kim, HJ, Kitazawa, T, Lamberts, A, Liang, H, Linn, SN, Litfin, T, Liusuo, W, Lygirou, V, Mahato, AK, Mai, Z-M, Major, RW, Mali, S, Mallis, P, Mao, W, Marvin-Dowle, K, Mason, LD, Merideth, B, Merino-Plaza, MJ, Merlaen, B, Messina, R, Mishra, AK, Muhammad, J, Musinguzi, C, Nanou, A, Naqash, A, Nguyen, JT, Nguyen, TTH, Ni, D, Nida, Notcovich, S, Ohst, B, Ollivier, QR, Osses, DF, Peng, X, Plantinga, A, Pulia, M, Rafiq, M, Raman, A, Raucher-Chene, D, Rawski, R, Ray, A, Razak, LA, Rudolf, K, Rusch, P, Sadoine, ML, Schmidt, A, Schurr, R, Searles, S, Sharma, S, Sheehan, B, Shi, C, Shohayeb, B, Sommerlad, A, Strehlow, J, Sun, X, Sundar, R, Taherzadeh, G, Tahir, NDM, Tang, J, Testa, J, Tian, Z, Tingting, Q, Verheijen, GP, Vickstrom, C, Wang, T, Wang, X, Wang, Z, Wei, P, Wilson, A, Wyart, Yassine, A-A, Yousefzadeh, A, Zare, A, Zeng, Z, Zhang, H, Zhou, J, Zhu, D, Adamo, V, Adeyemo, AA, Aggelidou, M, Al-Owaifeer, AM, Al-Riyami, AZ, Alzghari, SK, Andersen, V, Angus, K, Asaduzzaman, M, Asady, H, Ato, D, Bai, X, Baines, RL, Ballantyne, M, Ban, B, Beck, J, Ben-Nafa, W, Black, E, Blancher, A, Blankstein, R, Bodagh, N, Borges, PAV, Brooks, A, Brox-Ponce, J, Brunetti, A, Canham, CD, Carninci, P, Carvajal, R, Chang, SC, Chao, J, Chatterjee, P, Chhatriwalla, AK, Chikowe, I, Chuang, T-J, Collevatti, RG, Valera-Cornejo, DA, Cuenda, A, Dao, M, Dauga, D, Deng, Z, Devkota, K, Doan, LV, Elewa, YHA, Fan, D, Faruk, M, Feifei, S, Ferguson, TS, Fleres, F, Foster, EJ, Foster, CS, Furer, T, Gao, Y, Garcia-Rivera, EJ, Gazdar, A, George, RB, Ghosh, S, Gianchecchi, E, Gleason, JM, Hackshaw, A, Hall, A, Hall, R, Harper, P, Hogg, WE, Huang, G, Hunter, KE, IJzerman, AP, Jesus, C, Jian, G, Lewis, JS, Kanj, SS, Kaur, H, Kheir, F, Kichatova, VS, Kiyani, M, Klein, R, Kovesi, T, Kraschnewski, JL, Kumar, AP, Labutin, D, Lazo-Langner, A, Leclercq, G, Li, M, Li, Q, Li, T, Liao, W-T, Liao, Z-Y, Lin, J, Lizer, J, Lobreglio, G, Lowies, C, Lu, C, Majeed, H, Martin, A, Martinez-Sobrido, L, Meresh, E, Middelveen, M, Mohebbi, A, Mota, J, Mozaheb, Z, Muyaya, L, Nandhakumar, A, Ng, SHX, Obeidat, M, Oh, D-H, Owais, M, Pace-Asciak, P, Panwar, A, Patterson, C, Penagos-Tabaree, F, Pianosi, PT, Pinzi, V, Pridans, C, Psaroulaki, A, Pujala, RK, Pulido-Arjona, L, Qi, P-F, Rahman, P, Rai, NK, Rassaf, T, Refardt, J, Ricciardi, W, Riess, O, Rovas, A, Sacks, FM, Saleh, S, Sampson, C, Schmutz, A, Sepanski, R, Sharma, N, Spearman, P, Subramaniapillai, M, Swali, R, Tan, CM, Tellechea, JI, Thomas, L-M, Tong, X, Veys, R, Vitriol, V, Wang, H-D, Waugh, J, Webb, SA, Williams, BA, Workman, AD, Xiang, T, Xie, L-X, Xu, T, Yang, C, Yoon, JG, Yuan, CM, Zaritsky, A, Zhao, H, Zuckerman, H, Lyu, R, Pullan, W, and Zhou, Y
Published: 2019

41. Molecular techniques and their limitations shape our view of the holobiont

Author: Cooke, I, Mead, O, Whalen, C, Boote, C, Moya, A, Ying, H, Robbins, S, Strugnell, JM, Darling, A, Miller, D, Voolstra, CR, Adamska, M, Cooke, I, Mead, O, Whalen, C, Boote, C, Moya, A, Ying, H, Robbins, S, Strugnell, JM, Darling, A, Miller, D, Voolstra, CR, and Adamska, M
Abstract: © 2019 Elsevier GmbH It is now recognised that the biology of almost any organism cannot be fully understood without recognising the existence and potential functional importance of associated microbes. Arguably, the emergence of this holistic viewpoint may never have occurred without the development of a crucial molecular technique, 16S rDNA amplicon sequencing, which allowed microbial communities to be easily profiled across a broad range of contexts. A diverse array of molecular techniques are now used to profile microbial communities, infer their evolutionary histories, visualise them in host tissues, and measure their molecular activity. In this review, we examine each of these categories of measurement and inference with a focus on the questions they make tractable, and the degree to which their capabilities and limitations shape our view of the holobiont.
Published: 2019

42. Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches

Author: Jaspers, C, Fraune, S, Arnold, AE, Miller, DJ, Bosch, TCG, Voolstra, CR, Jaspers, C, Fraune, S, Arnold, AE, Miller, DJ, Bosch, TCG, and Voolstra, CR
Published: 2019

43. Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis (vol 1, 95, 2018)

Author: Liu, H, Stephens, TG, Gonzalez-Pech, RA, Beltran, VH, Lapeyre, B, Bongaerts, P, Cooke, I, Aranda, M, Bourne, DG, Foret, S, Miller, DJ, van Oppen, MJH, Voolstra, CR, Ragan, MA, Chan, CX, Liu, H, Stephens, TG, Gonzalez-Pech, RA, Beltran, VH, Lapeyre, B, Bongaerts, P, Cooke, I, Aranda, M, Bourne, DG, Foret, S, Miller, DJ, van Oppen, MJH, Voolstra, CR, Ragan, MA, and Chan, CX
Abstract: [This corrects the article DOI: 10.1038/s42003-018-0098-3.].
Published: 2018

44. Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis

Author: Liu, H, Stephens, TG, Gonzalez-Pech, RA, Beltran, VH, Lapeyre, B, Bongaerts, P, Cooke, I, Aranda, M, Bourne, DG, Foret, S, Miller, DJ, van Oppen, MJH, Voolstra, CR, Ragan, MA, Chan, CX, Liu, H, Stephens, TG, Gonzalez-Pech, RA, Beltran, VH, Lapeyre, B, Bongaerts, P, Cooke, I, Aranda, M, Bourne, DG, Foret, S, Miller, DJ, van Oppen, MJH, Voolstra, CR, Ragan, MA, and Chan, CX
Abstract: Symbiosis between dinoflagellates of the genus Symbiodinium and reef-building corals forms the trophic foundation of the world's coral reef ecosystems. Here we present the first draft genome of Symbiodinium goreaui (Clade C, type C1: 1.03 Gbp), one of the most ubiquitous endosymbionts associated with corals, and an improved draft genome of Symbiodinium kawagutii (Clade F, strain CS-156: 1.05 Gbp) to further elucidate genomic signatures of this symbiosis. Comparative analysis of four available Symbiodinium genomes against other dinoflagellate genomes led to the identification of 2460 nuclear gene families (containing 5% of Symbiodinium genes) that show evidence of positive selection, including genes involved in photosynthesis, transmembrane ion transport, synthesis and modification of amino acids and glycoproteins, and stress response. Further, we identify extensive sets of genes for meiosis and response to light stress. These draft genomes provide a foundational resource for advancing our understanding of Symbiodinium biology and the coral-algal symbiosis.
Published: 2018

45. Corrigendum: Using aiptasia as a model to study metabolic interactions in cnidarian-Symbiodinium symbioses [Front. Physiol, 9, (2018) (214)] doi: 10.3389/fphys.2018.00214

Author: Rädecker, N, Raina, JB, Pernice, M, Perna, G, Guagliardo, P, Kilburn, MR, Aranda, M, Voolstra, CR, Rädecker, N, Raina, JB, Pernice, M, Perna, G, Guagliardo, P, Kilburn, MR, Aranda, M, and Voolstra, CR
Abstract: © 2018 Rädecker, Raina, Pernice, Perna, Guagliardo, Kilburn, Aranda and Voolstra. During submission of the final version of the manuscript for publication, a previous version of Figure 3 was accidentally uploaded. The labeling of this previous Figure version does not match the annotation in the figure legend. The correct version of Figure 3 and its legend appear below. The authors sincerely apologize for the error. This error does not change the scientific conclusions of the research article.
Published: 2018

46. Thermal refugia against coral bleaching throughout the northern Red Sea

Author: Osman, EO, Smith, DJ, Ziegler, M, Kürten, B, Conrad, C, El-Haddad, KM, Voolstra, CR, Suggett, DJ, Osman, EO, Smith, DJ, Ziegler, M, Kürten, B, Conrad, C, El-Haddad, KM, Voolstra, CR, and Suggett, DJ
Abstract: © 2017 John Wiley & Sons Ltd Tropical reefs have been impacted by thermal anomalies caused by global warming that induced coral bleaching and mortality events globally. However, there have only been very few recordings of bleaching within the Red Sea despite covering a latitudinal range of 15° and consequently it has been considered a region that is less sensitive to thermal anomalies. We therefore examined historical patterns of sea surface temperature (SST) and associated anomalies (1982–2012) and compared warming trends with a unique compilation of corresponding coral bleaching records from throughout the region. These data indicated that the northern Red Sea has not experienced mass bleaching despite intensive Degree Heating Weeks (DHW) of >15°C-weeks. Severe bleaching was restricted to the central and southern Red Sea where DHWs have been more frequent, but far less intense (DHWs <4°C-weeks). A similar pattern was observed during the 2015–2016 El Niño event during which time corals in the northern Red Sea did not bleach despite high thermal stress (i.e. DHWs >8°C-weeks), and bleaching was restricted to the central and southern Red Sea despite the lower thermal stress (DHWs < 8°C-weeks). Heat stress assays carried out in the northern (Hurghada) and central (Thuwal) Red Sea on four key reef-building species confirmed different regional thermal susceptibility, and that central Red Sea corals are more sensitive to thermal anomalies as compared to those from the north. Together, our data demonstrate that corals in the northern Red Sea have a much higher heat tolerance than their prevailing temperature regime would suggest. In contrast, corals from the central Red Sea are close to their thermal limits, which closely match the maximum annual water temperatures. The northern Red Sea harbours reef-building corals that live well below their bleaching thresholds and thus we propose that the region represents a thermal refuge of global importance.
Published: 2018

47. Corrigendum: Using aiptasia as a model to study metabolic interactions in cnidarian-Symbiodinium symbioses [Front. Physiol, 9, (2018) (214)] doi: 10.3389/fphys.2018.00214

Author: Rädecker, N, Raina, JB, Pernice, M, Perna, G, Guagliardo, P, Kilburn, MR, Aranda, M, Voolstra, CR, Rädecker, N, Raina, JB, Pernice, M, Perna, G, Guagliardo, P, Kilburn, MR, Aranda, M, and Voolstra, CR
Abstract: © 2018 Rädecker, Raina, Pernice, Perna, Guagliardo, Kilburn, Aranda and Voolstra. During submission of the final version of the manuscript for publication, a previous version of Figure 3 was accidentally uploaded. The labeling of this previous Figure version does not match the annotation in the figure legend. The correct version of Figure 3 and its legend appear below. The authors sincerely apologize for the error. This error does not change the scientific conclusions of the research article.
Published: 2018

48. Thermal refugia against coral bleaching throughout the northern Red Sea

Author: Osman, EO, Smith, DJ, Ziegler, M, Kürten, B, Conrad, C, El-Haddad, KM, Voolstra, CR, Suggett, DJ, Osman, EO, Smith, DJ, Ziegler, M, Kürten, B, Conrad, C, El-Haddad, KM, Voolstra, CR, and Suggett, DJ
Abstract: © 2017 John Wiley & Sons Ltd Tropical reefs have been impacted by thermal anomalies caused by global warming that induced coral bleaching and mortality events globally. However, there have only been very few recordings of bleaching within the Red Sea despite covering a latitudinal range of 15° and consequently it has been considered a region that is less sensitive to thermal anomalies. We therefore examined historical patterns of sea surface temperature (SST) and associated anomalies (1982–2012) and compared warming trends with a unique compilation of corresponding coral bleaching records from throughout the region. These data indicated that the northern Red Sea has not experienced mass bleaching despite intensive Degree Heating Weeks (DHW) of >15°C-weeks. Severe bleaching was restricted to the central and southern Red Sea where DHWs have been more frequent, but far less intense (DHWs <4°C-weeks). A similar pattern was observed during the 2015–2016 El Niño event during which time corals in the northern Red Sea did not bleach despite high thermal stress (i.e. DHWs >8°C-weeks), and bleaching was restricted to the central and southern Red Sea despite the lower thermal stress (DHWs < 8°C-weeks). Heat stress assays carried out in the northern (Hurghada) and central (Thuwal) Red Sea on four key reef-building species confirmed different regional thermal susceptibility, and that central Red Sea corals are more sensitive to thermal anomalies as compared to those from the north. Together, our data demonstrate that corals in the northern Red Sea have a much higher heat tolerance than their prevailing temperature regime would suggest. In contrast, corals from the central Red Sea are close to their thermal limits, which closely match the maximum annual water temperatures. The northern Red Sea harbours reef-building corals that live well below their bleaching thresholds and thus we propose that the region represents a thermal refuge of global importance.
Published: 2018

49. Engineering strategies to decode and enhance the genomes of coral symbionts

Author: Levin, RA, Voolstra, CR, Agrawal, S, Steinberg, PD, Suggett, DJ, van Oppen, MJH, Levin, RA, Voolstra, CR, Agrawal, S, Steinberg, PD, Suggett, DJ, and van Oppen, MJH
Abstract: © 2017 Levin, Voolstra, Agrawal, Steinberg, Suggett and van Oppen. Elevated sea surface temperatures from a severe and prolonged El Niño event (2014-2016) fueled by climate change have resulted in mass coral bleaching (loss of dinoflagellate photosymbionts, Symbiodinium spp., from coral tissues) and subsequent coral mortality, devastating reefs worldwide. Genetic variation within and between Symbiodinium species strongly influences the bleaching tolerance of corals, thus recent papers have called for genetic engineering of Symbiodinium to elucidate the genetic basis of bleaching-relevant Symbiodinium traits. However, while Symbiodinium has been intensively studied for over 50 years, genetic transformation of Symbiodinium has seen little success likely due to the large evolutionary divergence between Symbiodinium and other model eukaryotes rendering standard transformation systems incompatible. Here, we integrate the growing wealth of Symbiodinium next-generation sequencing data to design tailored genetic engineering strategies. Specifically, we develop a testable expression construct model that incorporates endogenous Symbiodinium promoters, terminators, and genes of interest, as well as an internal ribosomal entry site from a Symbiodinium virus. Furthermore, we assess the potential for CRISPR/Cas9 genome editing through new analyses of the three currently available Symbiodinium genomes. Finally, we discuss how genetic engineering could be applied to enhance the stress tolerance of Symbiodinium, and in turn, coral reefs.
Published: 2017

50. Engineering Strategies to Decode and Enhance the Genomes of Coral Symbionts

Author: Levin, RA, Voolstra, CR, Agrawal, S, Steinberg, PD, Suggett, DJ, van Oppen, MJH, Levin, RA, Voolstra, CR, Agrawal, S, Steinberg, PD, Suggett, DJ, and van Oppen, MJH
Abstract: Elevated sea surface temperatures from a severe and prolonged El Niño event (2014-2016) fueled by climate change have resulted in mass coral bleaching (loss of dinoflagellate photosymbionts, Symbiodinium spp., from coral tissues) and subsequent coral mortality, devastating reefs worldwide. Genetic variation within and between Symbiodinium species strongly influences the bleaching tolerance of corals, thus recent papers have called for genetic engineering of Symbiodinium to elucidate the genetic basis of bleaching-relevant Symbiodinium traits. However, while Symbiodinium has been intensively studied for over 50 years, genetic transformation of Symbiodinium has seen little success likely due to the large evolutionary divergence between Symbiodinium and other model eukaryotes rendering standard transformation systems incompatible. Here, we integrate the growing wealth of Symbiodinium next-generation sequencing data to design tailored genetic engineering strategies. Specifically, we develop a testable expression construct model that incorporates endogenous Symbiodinium promoters, terminators, and genes of interest, as well as an internal ribosomal entry site from a Symbiodinium virus. Furthermore, we assess the potential for CRISPR/Cas9 genome editing through new analyses of the three currently available Symbiodinium genomes. Finally, we discuss how genetic engineering could be applied to enhance the stress tolerance of Symbiodinium, and in turn, coral reefs.
Published: 2017

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