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The algal endosymbiont Durusdinium trenchii enhances the resilience of coral reefs under thermal stress. D. trenchii can live freely or in endosymbiosis, and the analysis of genetic markers suggests that this species has undergone whole-genome duplication (WGD). However, the evolutionary mechanisms that underpin the thermotolerance of this species are largely unknown. Here, we present genome assemblies for two D. trenchii isolates, confirm WGD in these taxa, and examine how selection has shaped the duplicated genome regions using gene expression data. We assess how the free-living versus endosymbiotic lifestyles have contributed to the retention and divergence of duplicated genes, and how these processes have enhanced the thermotolerance of D. trenchii. Our combined results suggest that lifestyle is the driver of post-WGD evolution in D. trenchii, with the free-living phase being the most important, followed by endosymbiosis. Adaptations to both lifestyles likely enabled D. trenchii to provide enhanced thermal stress protection to the host coral.

The coral holobiont is underpinned by complex metabolic exchanges between different symbiotic partners, which are impacted by environmental stressors. The chemical diversity of the compounds produced by the holobiont is high and includes primary and secondary metabolites, as well as volatiles. However, metabolites and volatiles have only been characterised in isolation so far. Here, we applied a paired metabolomic-volatilomic approach to characterise holistically the chemical response of the holobiont under stress. Montipora mollis fragments were subjected to high-light stress (8-fold higher than the controls) for 30 min. Photosystem II (PSII) photochemical efficiency values were 7-fold higher in control versus treatment corals immediately following high-light exposure, but returned to pre-stress levels after 30 min of recovery. Under high-light stress, we identified an increase in carbohydrates (> 5-fold increase in arabinose and fructose) and saturated fatty acids (7-fold increase in myristic and oleic acid), together with a decrease in fatty acid derivatives in both metabolites and volatiles (e.g., 80% decrease in oleamide and nonanal), and other antioxidants (~ 85% decrease in sorbitol and galactitol). These changes suggest short-term light stress induces oxidative stress. Correlation analysis between volatiles and metabolites identified positive links between sorbitol, galactitol, six other metabolites and 11 volatiles, with four of these compounds previously identified as antioxidants. This suggests that these 19 compounds may be related and share similar functions. Taken together, our findings demonstrate how paired metabolomics-volatilomics may illuminate broader metabolic shifts occurring under stress and identify linkages between uncharacterised compounds to putatively determine their functions.

Coral propagation and out-planting based restoration approaches are increasingly being applied to assist natural recovery of coral reefs. However, many restoration methods rely on plastic zip-ties to secure coral material which is potentially problematic for the marine environment. Plastic-free biodegradable alternatives may however pose unique risks to coral-associated bacterial communities integral to coral health. Therefore, to identify whether biodegradable materials differentially impact coral-associated bacterial communities we examined Acropora millepora coral-associated bacterial communities during propagation in two experiments on the Great Barrier Reef. Coral fragments were secured to coral nurseries with conventional plastic, metal, or biodegradable (polyester and polycaprolactone) ties. Tie failure and coral-associated bacterial communities were then characterized over six months. Minimal coral mortality was observed (3.6%-8%) and all ties had low failure rates (0%-4.2%) except for biodegradable polyester ties (29.2% failure). No differences were observed between coral-associated bacterial communities of fragments secured with different ties, and no proliferation of putatively pathogenic bacteria was recorded. Overall, our findings suggest that reducing reliance on conventional plastic is feasible through transitions to biodegradable materials, without any notable impacts on coral-associated bacterial communities. However, we caution the need to examine more coral taxa of different morphologies and new plastic-free materials prior to application.

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.

Cnidarian-microalgae (Family: Symbiodiniaceae) endosymbiotic relationships are central to the success of reef building corals, particularly shaping stress tolerance and capacity to adapt to ever-changing environmental conditions. Studies have particularly examined Symbiodiniaceae susceptibility (and adaptation) to thermal stress to aid reef management as reef temperatures continue to rise. Thermal Performance Curves (TPCs) have previously been well studied to resolve how changing temperatures influence organism competitive fitness but have only recently been applied to corals and never before to Symbiodiniaceae. We therefore developed and applied rapid assay TPCs to 7 Symbiodiniaceae isolates (spanning 5 genera) from different reef origins. Isolates were exposed to temperature gradients, ramping up (26-35 °C) and down (26-17 °C) by 1 °C every 3 days. Photophysiological performance (maximum and effective photochemical efficiency, Fv/Fm and Fq´/Fm´) measured at each temperature was used to fit TPC algorithms describing temperature for optimal performance (Topt), critical thermal minimum or maximum (Ctmin or Ctmax), and thermal performance breadth (Tbr). TPC characteristics varied across the isolates revealing diverse performance ranges. Fv/Fm-derived Topt across all 7 isolates was 25.84 °C, with isolate WT3.2 (Symbiodinium spp.) returning the highest overall Topt (26.89 °C) and Ctmax (36.63 °C) values. In contrast, isolate RT141 (Breviolum psygmophilum) had the greatest Tbr (16.15 °C). As such, Fv/Fm-derived TPCs revealed thermal “generalism” of the temperate originating RT141 in comparison to more thermal “specialism” of WT3.2 originating from a hot tropical mangrove lagoon. Thermal characteristics were more varied across isolates when fitting TPCs to the effective photochemical efficiencies (Fq´/Fm´). We discuss how TPC-based characteristics are ultimately operationally defined in terms of thermal perturbation, choice of TPC algorithm and physiological descriptor, a

Coral propagation and out-planting are becoming commonly adopted as part of reef stewardship strategies aimed at improving reef resilience through enhanced natural recovery and rehabilitation. The coral microbiome has a crucial role in the success of the coral holobiont and can be impacted shortly after out-planting. However, long-term characterisation of the out-plant microbiome in relation to out-plant survival, and how these properties vary across reef sites, is unexplored. Therefore, at three reef sites on Opal Reef, Great Barrier Reef (Mojo, Sandbox and Rayban, 16°12′18″S 145°53′54″E), we examined bacterial communities associated with out-planted Acropora millepora coral and monitored coral survival over 12 months (February 2021–22). Bacterial communities of out-planted corals exhibited significant changes from donor colonies 7 days to 1.5 months after out-planting. Further, bacterial community composition differed for sites Sandbox and Rayban with low overall survival (0–43%) versus Mojo with higher overall survival (47–75%). After initial dissimilarity in bacterial communities of out-plants across sites at 1.5 months, and despite changes within sites over time, out-plants exhibited similar microbial communities across sites at 7 days and 6, 9 and 12 months. We hypothesise these trends reflect how bacterial communities are shaped by rapid changes in local environmental characteristics (e.g. from source to out-planting site), where out-plant bacterial communities ‘conform’ to out-planting site conditions. After initial changes, out-plant bacterial communities may then be under the influence of global environmental conditions—such as annual trends in temperature across seasons. Such outcomes indicate the importance of site selection in shaping initial coral bacterial communities and subsequent out-plant success. Importantly, continued differences in out-plant survival trajectory but similar bacterial communities across sites after 1.5 months indicate that other

Symbiodiniaceae form associations with extra- and intracellular bacterial symbionts, both in culture and in symbiosis with corals. Bacterial associates can regulate Symbiodiniaceae fitness in terms of growth, calcification and photophysiology. However, the influence of these bacteria on interactive stressors, such as temperature and light, which are known to influence Symbiodiniaceae physiology, remains unclear. Here, we examined the photophysiological response of two Symbiodiniaceae species (Symbiodinium microadriaticum and Breviolum minutum) cultured under acute temperature and light stress with specific bacterial partners from their microbiome (Labrenzia (Roseibium) alexandrii, Marinobacter adhaerens or Muricauda aquimarina). Overall, bacterial presence positively impacted Symbiodiniaceae core photosynthetic health (photosystem II [PSII] quantum yield) and photoprotective capacity (non-photochemical quenching; NPQ) compared to cultures with all extracellular bacteria removed, although specific benefits were variable across Symbiodiniaceae genera and growth phase. Symbiodiniaceae co-cultured with M. aquimarina displayed an inverse NPQ response under high temperatures and light, and those with L. alexandrii demonstrated a lowered threshold for induction of NPQ, potentially through the provision of antioxidant compounds such as zeaxanthin (produced by Muricauda spp.) and dimethylsulfoniopropionate (DMSP; produced by this strain of L. alexandrii). Our co-culture approach empirically demonstrates the benefits bacteria can deliver to Symbiodiniaceae photochemical performance, providing evidence that bacterial associates can play important functional roles for Symbiodiniaceae.

Tourism-led stewardship of Great Barrier Reef (GBR) sites has implemented upscaling of coral propagation and out-planting practices. Incorporating ecological monitoring into restoration practices has long been acknowledged as a vital component of reef restoration projects – thereby demonstrating success in relation to improved ecosystem function within impacted reefs. As such, one goal for this tourism-led stewardship project was to identify whether and how activity increased coral cover and target species populations within high-value tourism sites. We therefore investigated coral cover and relative cover of commonly out-planted genera within seven tourism sites over six reefs on the northern GBR via benthic surveys, both prior to the commencement of out-planting activities in August 2019, and again in August 2021. Over this 24-month time frame, out-planting intensity varied between 3970 and 84 out-plants within marked areas (with no propagation activity conducted within corresponding control areas) across sites. Within all out-planting sites, > 65 % of out-plants were Acropora species. One reef showed a significant increase in hard coral cover – 10.3 % (p = 0.016) – at out-planting areas compared to control areas by August 2021. At this same reef, proportions of total coral cover attributed to Acropora species were higher within the out-planting site compared to the control site. Despite variability in coral community responses observed across reef site/operators, we have demonstrated how coral propagation via this tourism-led stewardship model has the potential to increase hard coral cover within some out-planting sites, particularly of commonly out-planted genera.

Anthropogenic stressors continue to escalate worldwide, driving unprecedented declines in reef environmental conditions and coral health. One approach to better understand how corals can function in the future is to examine coral populations that thrive within present day naturally extreme habitats. We applied untargeted metabolomics (gas chromatography-mass spectrometry (GC-MS)) to contrast metabolite profiles of Pocillopora acuta colonies from hot, acidic and deoxygenated mangrove environments versus those from adjacent reefs. Under ambient temperatures, P. acuta predominantly associated with endosymbionts of the genera Cladocopium (reef) or Durusdinium (mangrove), exhibiting elevated metabolism in mangrove through energy-generating and biosynthesis pathways compared to reef populations. Under transient heat stress, P. acuta endosymbiont associations were unchanged. Reef corals bleached and exhibited extensive shifts in symbiont metabolic profiles (whereas host metabolite profiles were unchanged). By contrast, mangrove populations did not bleach and solely the host metabolite profiles were altered, including cellular responses in inter-partner signalling, antioxidant capacity and energy storage. Thus mangrove P. acuta populations resist periodically high-temperature exposure via association with thermally tolerant endosymbionts coupled with host metabolic plasticity. Our findings highlight specific metabolites that may be biomarkers of heat tolerance, providing novel insight into adaptive coral resilience to elevated temperatures.

Bacteria are key contributors to microalgae resource acquisition, competitive performance, and functional diversity, but their potential metabolic interactions with coral microalgal endosymbionts (Symbiodiniaceae) have been largely overlooked. Here, we show that altering the bacterial composition of two widespread Symbiodiniaceae species, during their free-living stage, results in a significant shift in their cellular metabolism. Indeed, the abundance of monosaccharides and the key phytohormone indole-3-acetic acid (IAA) were correlated with the presence of specific bacteria, including members of the Labrenzia (Roseibium) and Marinobacter genera. Single-cell stable isotope tracking revealed that these two bacterial genera are involved in reciprocal exchanges of carbon and nitrogen with Symbiodiniaceae. We identified the provision of IAA by Labrenzia and Marinobacter, and this metabolite caused a significant growth enhancement of Symbiodiniaceae. By unravelling these interkingdom interactions, our work demonstrates how specific bacterial associates fundamentally govern Symbiodiniaceae fitness.

Humans have long sought to restore species but little attention has been directed at how to best select a subset of foundation species for maintaining rich assemblages that support ecosystems, like coral reefs and rainforests, which are increasingly threatened by environmental change. We propose a two-part hedging approach that selects optimized sets of species for restoration. The first part acknowledges that biodiversity supports ecosystem functions and services, and so it ensures precaution against loss by allocating an even spread of phenotypic traits. The second part maximizes species and ecosystem persistence by weighting species based on characteristics that are known to improve ecological persistence—for example abundance, species range and tolerance to environmental change. Using existing phenotypic-trait and ecological data for reef building corals, we identified sets of ecologically persistent species by examining marginal returns in occupancy of phenotypic trait space. We compared optimal sets of species with those from the world's southern-most coral reef, which naturally harbours low coral diversity, to show these occupy much of the trait space. Comparison with an existing coral restoration program indicated that current corals used for restoration only cover part of the desired trait space and programs may be improved by including species with different traits. Synthesis and applications. While there are many possible criteria for selecting species for restoration, the approach proposed here addresses the need to insure against unpredictable losses of ecosystem services by focusing on a wide range of phenotypic traits and ecological characteristics. Furthermore, the flexibility of the approach enables the functional goals of restoration to vary depending on environmental context, stakeholder values, and the spatial and temporal scales at which meaningful impacts can be achieved.

Diatoms are major producers of carbon and energy in aquatic ecosystems, however their ability to rapidly and successfully acclimate to wide ranging irradiances is poorly understood at the biochemical level. We applied complementary transcriptomic and metabolomic approaches using the model centric diatom Thalassiosira pseudonana to understand mechanisms regulating cell acclimation and growth under high and low light intensities. The integration of these omics data revealed specific mechanisms that shifted carbon and energy fluxes in T. pseudonana depending on light-driven growth rate. To support a growth rate of >1 d−1 in high light, cells upregulated metabolic pathways involved in the production of long chain fatty acids, glycolic acid, and carbohydrates. Under low light, cells maintained a growth rate of ≤0.2 d−1 by conserving photosynthetic energy through upregulation of carbon retention pathways (e.g., gluconeogenesis, glyoxylate cycle). The few significant metabolites detected in low light acclimated cells were associated with light harvesting, energy storage, and signalling. In particular, our metabolite data revealed that eicosanoic acid, a metabolite commonly involved in cellular signalling, may poise light limited cells for fast metabolic remodelling with improving light conditions. The combined physiological, gene expression and metabolite profiling data revealed key metabolic switch points that underpin diatom success and could be leveraged in cell-based models for predictions and manipulations of cell growth or bio-production.

The mutualistic cnidarian-dinoflagellate symbiosis underpins the evolutionary success of stony corals and the persistence of coral reefs. However, a molecular understanding of the signalling events that lead to the successful establishment and maintenance of this symbiosis remains unresolved. For example, the phosphatidylinositol (PI) signalling pathway has been implicated during the establishment of multiple mutualistic and parasitic interactions across the kingdoms of life, yet its role within the cnidarian-dinoflagellate symbiosis remains unexplored. Here, we aimed to confirm the presence and assess the specific enzymatic composition of the PI signalling pathway across cnidaria and dinoflagellates by compiling 21 symbiotic anthozoan (corals and sea anemones) and 28 symbiotic dinoflagellate (Symbiodiniaceae) transcriptomic and genomic datasets and querying genes related to this pathway. Presence or absence of PI-kinase and PI-phosphatase orthologs were also compared between a broad sampling of taxonomically related symbiotic and non-symbiotic species. Across the symbiotic anthozoans analysed, there was a complete and highly conserved PI pathway, analogous to the pathway found in model eukaryotes. The Symbiodiniaceae pathway showed similarities to its sister taxon, the Apicomplexa, with the absence of PI 4-phosphatases. However, conversely to Apicomplexa, there was also an expansion of homologs present in the PI5-phosphatase and PI5-kinase groups, with unique Symbiodiniaceae proteins identified that are unknown from non-symbiotic unicellular organisms. Additionally, we aimed to unravel the putative functionalities of the PI signalling pathway in this symbiosis by analysing phosphoinositide (PIP)-binding proteins. Analysis of phosphoinositide (PIP)-binding proteins showed that, on average, 2.23 and 1.29% of the total assemblies of anthozoan and Symbiodiniaceae, respectively, have the potential to bind to PIPs. Enrichment of Gene Ontology (GO) terms associated with p

The symbiosis between cnidarians and dinoflagellates underpins the success of reef-building corals in otherwise nutrient-poor habitats. Alterations to symbiotic state can perturb metabolic homeostasis and thus alter the release of biogenic volatile organic compounds (BVOCs). While BVOCs can play important roles in metabolic regulation and signalling, how the symbiotic state affects BVOC output remains unexplored. We therefore characterised the suite of BVOCs that comprise the volatilome of the sea anemone Exaiptasia diaphana ('Aiptasia') when aposymbiotic and in symbiosis with either its native dinoflagellate symbiont Breviolum minutum or the non-native symbiont Durusdinium trenchii. In parallel, the bacterial community structure in these different symbiotic states was fully characterised to resolve the holobiont microbiome. Based on rRNA analyses, 147 unique amplicon sequence variants (ASVs) were observed across symbiotic states. Furthermore, the microbiomes were distinct across the different symbiotic states: bacteria in the family Vibrionaceae were the most abundant in aposymbiotic anemones; those in the family Crocinitomicaceae were the most abundant in anemones symbiotic with D. trenchii; and anemones symbiotic with B. minutum had the highest proportion of low-abundance ASVs. Across these different holobionts, 142 BVOCs were detected and classified into 17 groups based on their chemical structure, with BVOCs containing multiple functional groups being the most abundant. Isoprene was detected in higher abundance when anemones hosted their native symbiont, and dimethyl sulphide was detected in higher abundance in the volatilome of both Aiptasia-Symbiodiniaceae combinations relative to aposymbiotic anemones. The volatilomes of aposymbiotic anemones and anemones symbiotic with B. minutum were distinct, while the volatilome of anemones symbiotic with D. trenchii overlapped both of the others. Collectively, our results are consistent with previous reports that D. tre

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.

Coral reef restoration activity is accelerating worldwide in efforts to offset the rate of reef health declines. Many advances have already been made in restoration practices centred on coral biology (coral restoration), and particularly those that look to employ the high adaptive state and capacity of corals in order to ensure that efforts rebuilding coral biomass also equip reefs with enhanced resilience to future stress. We horizon scan the state-of-play for the many coral restoration innovations already underway across the complex life cycle for corals that spans both asexual and sexual reproduction - assisted evolution (manipulations targeted to the coral host and host-associated microbes), biobanking, as well as scalable coral propagation and planting - and how these innovations are in different stages of maturity to support new 21st century reef management frameworks. Realising the potential for coral restoration tools as management aids undoubtedly rests on validating different approaches as their application continues to scale. Whilst the ecosystem service responses to increased scaling still largely remain to be seen, coral restoration has already delivered immense new understanding of coral and coral-associated microbial biology that has long lagged behind advances in other reef sciences.

The Symbiodiniaceae are a taxonomically and functionally diverse family of marine dinoflagellates. Their symbiotic relationship with invertebrates such as scleractinian corals has made them the focus of decades of research to resolve the underlying biology regulating their sensitivity to stressors, particularly thermal stress. Research to-date suggests that Symbiodiniaceae stress sensitivity is governed by a complex interplay between phylogenetic dependent and independent traits (diversity of characteristics of a species). Consequently, there is a need for datasets that simultaneously broadly resolve molecular and physiological processes under stressed and non-stressed conditions. Therefore, we provide a dataset simultaneously generating transcriptome, metabolome, and proteome data for three ecologically important Symbiodiniaceae isolates under nutrient replete growth conditions and two temperature treatments (ca. 26 °C and 32 °C). Elevated sea surface temperature is primarily responsible for coral bleaching events that occur when the coral-Symbiodiniaceae relationship has been disrupted. Symbiodiniaceae can strongly influence their host's response to thermal stress and consequently it is necessary to resolve drivers of Symbiodiniaceae heat stress tolerance. We anticipate these datasets to expand our understanding on the key genotypic and functional properties that influence the sensitivities of Symbiodiniaceae to thermal stress.

While coral reefs in Australia have historically been a showcase of conventional management informed by research, recent declines in coral cover have triggered efforts to innovate and integrate intervention and restoration actions into management frameworks. Here we outline the multi-faceted intervention approaches that have developed in Australia since 2017, from newly implemented in-water programs, research to enhance coral resilience and investigations into socio-economic perspectives on restoration goals. We describe in-water projects using coral gardening, substrate stabilisation, coral repositioning, macro-algae removal, and larval-based restoration techniques. Three areas of research focus are also presented to illustrate the breadth of Australian research on coral restoration, (1) the transdisciplinary Reef Restoration and Adaptation Program (RRAP), one of the world's largest research and development programs focused on coral reefs, (2) interventions to enhance coral performance under climate change, and (3) research into socio-cultural perspectives. Together, these projects and the recent research focus reflect an increasing urgency for action to confront the coral reef crisis, develop new and additional tools to manage coral reefs, and the consequent increase in funding opportunities and management appetite for implementation. The rapid progress in trialling and deploying coral restoration in Australia builds on decades of overseas experience, and advances in research and development are showing positive signs that coral restoration can be a valuable tool to improve resilience at local scales (i.e., high early survival rates across a variety of methods and coral species, strong community engagement with local stakeholders). RRAP is focused on creating interventions to help coral reefs at multiple scales, from micro scales (i.e., interventions targeting small areas within a specific reef site) to large scales (i.e., interventions targeting core ecosystem fu

Efforts to manage coral reef declines are increasingly turning towards in situ propagation of corals to aid reef recovery. Understanding the factors that influence ‘success’ throughout the propagation process is therefore critical to ensure efforts are viable and cost-effective, yet the extent to which propagation practices potentially impact the underlying coral biology remains unknown. Given growing evidence for the importance of the coral microbiome, we examined the influence of nursery-based propagation and out-planting on the bacterial communities of two coral species–Acropora millepora and Pocillopora verrucosa–increasingly propagated on the northern Great Barrier Reef (Opal Reef). Bacterial communities of coral fragments were characterised over four months of nursery propagation (sampling points: zero, seven and 125 days) and one month of subsequent out-planting (sampling points: zero, one and 30 days). Bacterial community structure differed between A. millepora and P. verrucosa throughout the experiment and species-specific temporal dynamics were observed during the transplantation of corals into nurseries and subsequent out-planting back to the reef. P. verrucosa bacterial community structure remained stable over time in the natural reef environment and within the nursery. In contrast, A. millepora bacterial communities within the nursery significantly changed over time, whereas those associated with source colonies within the natural reef environment remained unchanged. However, after one month of out-planting, the composition, richness and diversity of A. millepora bacterial communities were not statistically different to those associated with the source colonies. We interpret the transient shift of A. millepora bacterial communities within the nursery as an impact of distinctive environmental conditions in nurseries compared to natural reef settings, and the greater responsiveness of A. millepora bacterial communities to environmental change. Our observa

The establishment and maintenance of the symbiosis between a cnidarian host and its dinoflagellate symbionts is central to the success of coral reefs. To explore the metabolite production underlying this symbiosis, we focused on a group of low molecular weight secondary metabolites, biogenic volatile organic compounds (BVOCs). BVOCs are released from an organism or environment, and can be collected in the gas phase, allowing non-invasive analysis of an organism's metabolism (i.e. 'volatilomics'). We characterised volatile profiles of the sea anemone Aiptasia (Exaiptasia diaphana), a model system for cnidarian-dinoflagellate symbiosis, using comprehensive two-dimensional gas chromatography coupled with time-of-flight mass spectrometry. We compared volatile profiles between: (1) symbiotic anemones containing their native symbiont, Breviolum minutum; (2) aposymbiotic anemones; and (3) cultured isolates of B. minutum. Overall, 152 BVOCs were detected, and classified into 14 groups based on their chemical structure, the most numerous groups being alkanes and aromatic compounds. A total of 53 BVOCs were differentially abundant between aposymbiotic anemones and B. minutum cultures; 13 between aposymbiotic and symbiotic anemones; and 60 between symbiotic anemones and cultures of B. minutum. More BVOCs were differentially abundant between cultured and symbiotic dinoflagellates than between aposymbiotic and symbiotic anemones, suggesting that symbiosis may modify symbiont physiology more than host physiology. This is the first volatilome analysis of the Aiptasia model system and provides a foundation from which to explore how BVOC production is perturbed under environmental stress, and ultimately the role they play in this important symbiosis.

Coral reefs in Malaysia have been degraded by environmental and anthropogenic stressors, and enthusiasm for coral propagation aimed at site restoration is rapidly growing as a local management tool. However, coral propagation activities in the region are in their infancy and little data currently exists to guide and inform effective practices. We therefore established the first multi-taxa coral tree nursery (6 species and 300 fragments) in Malaysia and tracked survival and growth to determine the relative return-on-effort (RRE) over an approximately 14-month monitoring period. We observed differences in growth and survival among six coral species and were successful at benchmarking results against coral restoration operations globally and in the East Asian Seas region. Major findings include (1) overall ranges in species level survivorship of 34–94% and specific growth rate of 0.14–0.29%/day, leading to variable RRE scores among species, (2) variable growth rates among coral species based on seasonal changes in environmental conditions, (3) similar RRE scores to other nursery locations worldwide, which suggests effective practice, and (4) calculation of RRE scores for species not previously reported in nursery culture (Acropora florida, A. hoeksemai, and Echinopora horrida). Ultimately, our study supports previous findings that RRE is an effective technique for comparing coral nursery performance and offers valuable insight to guide future restoration activities in Malaysia.

High-latitude reefs are suboptimal coral habitats, but such habitats are increasingly considered to be potential refugia from climate change for range-shifting coral reef species. Notably, tropical reef fish have been observed along the south-east coast of Australia, but their establishment on temperate rocky reefs is currently limited by winter minimum temperatures and other resource needs, such as structurally complex habitats typical of tropical reefs. Recent expansion of the branching subtropical coral Pocillopora aliciae in rocky reefs near Sydney (34° S) could diversify the architectural structure of temperate marine environments, thereby providing potential shelter for tropical reef taxa in warming seas. Here, we investigated whether future environmental conditions (i.e. temperature increase) can influence the dominance of the subtropical branching coral P. aliciae over the resident encrusting coral Plesiastrea versipora in coastal Sydney by characterising physiological (e.g. metabolic stability) and behavioural (e.g. interspecific competitive hierarchy) traits that contribute to their competitive fitness. Our results suggest that a metabolic response, mediated by sterol and lipid metabolic pathways and provision of antioxidants, allows P. aliciae to reduce cellular stress and withstand exposure to short-term increased temperature. Conversely, P. versipora was more susceptible to heat exposure with no metabolic mediation observed. While P. versipora displayed greater aggressive behaviour when in direct contact with P. aliciae under all temperature conditions, the superior physiological and metabolic flexibility under increased temperatures of P. aliciae suggests that this species will likely outperform P. versipora under future increased temperatures. Such contrasting responses to environmental change would facilitate shifts in coral community and functional composition that could support further tropicalisation of coastal New South Wales.

[This corrects the article DOI: 10.1016/j.csbj.2021.11.036.].

Sessile invertebrates are frequently sampled and processed whole for downstream analyses. However, their apparent structural simplicity is deceptive as these organisms often harbour discrete compartments. These compartments have physicochemical conditions that differ markedly from neighbouring tissues, and that have likely evolved to support specific functions. Here, we argue that such compartments should be specifically targeted when characterising sessile invertebrate biology and we use the coral gastrovascular cavity to support our argument. This complex compartment displays steep and dynamic chemical gradients, harbours distinct microorganisms, and presumably plays a key role in coral biology. Disentangling the functions played by (and amongst) compartments will likely provide transformative insight into the biology of sessile invertebrates and their future under environmental change.

Coral bleaching has increasingly impacted reefs worldwide over the past four decades. Despite almost 40 years of research into the mechanistic, physiological, ecological, biophysical and climatic drivers of coral bleaching, metrics to allow comparison between ecological observations and experimental simulations still do not exist. Here we describe a novel metric - experimental Degree Heating Week (eDHW) - with which to standardise the persistently variable thermal conditions employed across experimental studies of coral bleaching by modify the widely used Degree Heating Week (DHW) metric used in ecological studies to standardise cumulative heat loading.

BACKGROUND: Elements are the basis of life on Earth, whereby organisms are essentially evolved chemical substances that dynamically interact with each other and their environment. Determining species elemental quotas (their elementome) is a key indicator for their success across environments with different resource availabilities. Elementomes remain undescribed for functionally diverse dinoflagellates within the family Symbiodiniaceae that includes coral endosymbionts. We used dry combustion and ICP-MS to assess whether Symbiodiniaceae (ten isolates spanning five genera Breviolum, Cladocopium, Durusdinium, Effrenium, Symbiodinium) maintained under long-term nutrient replete conditions have unique elementomes (six key macronutrients and nine micronutrients) that would reflect evolutionarily conserved preferential elemental acquisition. For three isolates we assessed how elevated temperature impacted their elementomes. Further, we tested whether Symbiodiniaceae conform to common stoichiometric hypotheses (e.g., the growth rate hypothesis) documented in other marine algae. This study considers whether Symbiodiniaceae isolates possess unique elementomes reflective of their natural ecologies, evolutionary histories, and resistance to environmental change. RESULTS: Symbiodiniaceae isolates maintained under long-term luxury uptake conditions, all exhibited highly divergent elementomes from one another, driven primarily by differential content of micronutrients. All N:P and C:P ratios were below the Redfield ratio values, whereas C:N was close to the Redfield value. Elevated temperature resulted in a more homogenised elementome across isolates. The Family-level elementome was (C19.8N2.6 P1.0S18.8K0.7Ca0.1) · 1000 (Fe55.7Mn5.6Sr2.3Zn0.8Ni0.5Se0.3Cu0.2Mo0.1V0.04) mmol Phosphorous-1 versus (C25.4N3.1P1.0S23.1K0.9Ca0.4) · 1000 (Fe66.7Mn6.3Sr7.2Zn0.8Ni0.4Se0.2Cu0.2Mo0.2V0.05) mmol Phosphorous -1 at 27.4 ± 0.4 °C and 30.7 ± 0.01 °C, respectively. Symbiodiniaceae isolates tested h

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.

Increasing anthropogenic pressure on coral reefs is creating an urgent need to understand how and where corals can proliferate both now and under future scenarios. Resolving environmental limits of corals has progressed through the accurate identification of corals’ ‘realised ecological niche’. Here we expand the ecological niche concept to account for corals’ ‘biogeochemical niche’ (BN), defined as the chemical space in which a coral is adapted to survive, and which is identifiable by a unique quantity and proportion of elements (termed “elementome”). BN theory has been commonly applied to other taxa, successfully predicting species distributions and stress responses by their elementomes. Here, we apply the BN theory to corals for the first time, by using dry combustion and inductively coupled plasma–mass spectrometry (ICP-MS) to determine five key macronutrients and thirteen trace elements of four diverse scleractinian coral species from the Great Barrier Reef (GBR): Acropora hyacinthus; Echinopora lamellosa; Pocillopora cf. meandrina; and Pocillopora cf. verrucosa. The elementomes were investigated in both host and Symbiodiniaceae, and the latter had the highest elemental concentrations (except molybdenum). Each coral species associated with distinct members of the genus Cladocopium (determined by ITS2 analysis) with photo-physiological data suggesting specialisation of Cladocopium functional biology. Distinct endosymbiont community structure and functioning between corals with different elementomes confirms that BN theory holds as metabolic compatibility alters across host–symbiont associations. Additional work is needed to understand the plasticity of coral elementomes, and in turn BN, over space and time to aid predictions on coral distribution and survival with environmental change.

The ecological success of tropical corals is regulated by symbiotic dinoflagellate algae (Symbiodiniaceae). Corals can associate with multiple Symbiodiniaceae species simultaneously, yet the conditions that permit Symbiodiniaceae cohabitation are not understood. We examined how corals self-shade their own tissues causing within-colony light gradients that drive Symbiodiniaceae photoacclimatory processes and positional genetic disparity. Paired light ‘exposed’ and ‘shaded’ samples from 20 coral species were collected from a shallow coral reef (Rarotonga, Cook Islands). Through active chlorophyll fluorometry, rapid light curves revealed that exposed Symbiodiniaceae exhibited 50% higher values in minimum saturating irradiances and demonstrated a shift towards preferential nonphotochemical quenching [1 – Q], consistent with higher overall light exposure. High-throughput or targeted DNA sequencing of ITS2 and psbAncr markers demonstrated that corals harboured distinct and/or differentially abundant Symbiodiniaceae ITS2 sequences (typically rare in relative abundance) or multiple ITS2 intragenomic variant profiles across shaded vs exposed regions. In Hydnophora cf. microconos, within-colony symbiont genetic disparity was positively correlated with the magnitude of difference in [1 – Q] utilisation. Together, these results suggest that within-colony light gradients produce distinct optical niches that enable symbiont cohabitation via photoadaptation, a phenomenon that is expected to increase the adaptive capacity of corals under future climates.

Among the most successful microeukaryotes to form mutualisms with animals are dinoflagellates in the family Symbiodiniaceae. These photosynthetic symbioses drive significant primary production and are responsible for the formation of coral reef ecosystems but are particularly sensitive when environmental conditions become extreme. Annual episodes of widespread coral bleaching (disassociation of the mutualistic partnership) and mortality are forecasted from the year 2060 under current trends of ocean warming. However, host cnidarians and dinoflagellate symbionts display exceptional genetic and functional diversity, and meaningful predictions of the future that embrace this biological complexity are difficult to make. A recent move to trait-based biology (and an understanding of how traits are shaped by the environment) has been adopted to move past this problem. The aim of this review is to: (1) provide an overview of the major cnidarian lineages that are symbiotic with Symbiodiniaceae; (2) summarise the symbiodiniacean genera associated with cnidarians with reference to recent changes in taxonomy and systematics; (3) examine the knowledge gaps in Symbiodiniaceae life history from a trait-based perspective; (4) review Symbiodiniaceae trait variation along three abiotic gradients (light, nutrients, and temperature); and (5) provide recommendations for future research of Symbiodiniaceae traits. We anticipate that a detailed understanding of traits will further reveal basic knowledge of the evolution and functional diversity of these mutualisms, as well as enhance future efforts to model stability and change in ecosystems dependent on cnidarian-dinoflagellate organisms.

Efforts are accelerating to protect and restore ecosystems globally. With trillions of dollars in ecosystem services at stake, no clear framework exists for developing or prioritizing approaches to restore coral reefs even as efforts and investment opportunities to do so grow worldwide. Restoration may buy time for climate change mitigation, but it lacks rigorous guidance to meet objectives of scalability and effectiveness. Lessons from restoration of terrestrial ecosystems can and should be rapidly adopted for coral reef restoration. We propose how the 10 golden rules of effective forest restoration can be translated to accelerate efforts to restore coral reefs based on established principles of resilience, management, and local stewardship. We summarize steps to undertake reef restoration as a management strategy in the context of the diverse ecosystem service values that coral reefs provide. Outlining a clear blueprint is timely as more stakeholders seek to undertake restoration as the UN Decade on Ecosystem Restoration begins.

Understanding the distribution and abundance of heat tolerant corals across seascapes is imperative for predicting responses to climate change and to support novel management actions. Thermal tolerance is variable in corals and intrinsic and extrinsic drivers of tolerance are not well understood. Traditional experimental evaluations of coral heat and bleaching tolerance typically involve ramp-and-hold experiments run across days to weeks within aquarium facilities with limits to colony replication. Field-based acute heat stress assays have emerged as an alternative experimental approach to rapidly quantify heat tolerance in many samples yet the role of key methodological considerations on the stress response measured remains unresolved. Here, we quantify the effects of coral fragment size, sampling time point, and physiological measures on the acute heat stress response in adult corals. The effect of fragment size differed between species (Acropora tenuis and Pocillopora damicornis). Most physiological parameters measured here declined over time (tissue colour, chlorophyll-a and protein content) from the onset of heating, with the exception of maximum photosynthetic efficiency (Fv/Fm) which was surprisingly stable over this time scale. Based on our experiments, we identified photosynthetic efficiency, tissue colour change, and host-specific assays such as catalase activity as key physiological measures for rapid quantification of thermal tolerance. We recommend that future applications of acute heat stress assays include larger fragments (> 9 cm2) where possible and sample between 10 and 24 h after the end of heat stress. A validated high-throughput experimental approach combined with cost-effective genomic and physiological measurements underpins the development of markers and maps of heat tolerance across seascapes and ocean warming scenarios.

For millennia, coastal and marine ecosystems have adapted and flourished in the Red Sea’s unique environment. Surrounded by deserts on all sides, the Red Sea is subjected to high dust inputs and receives very little freshwater input, and so harbors a high salinity. Coral reefs, seagrass meadows, and mangroves flourish in this environment and provide socio-economic and environmental benefits to the bordering coastlines and countries. Interestingly, while coral reef ecosystems are currently experiencing rapid decline on a global scale, those in the Red Sea appear to be in relatively better shape. That said, they are certainly not immune to the stressors that cause degradation, such as increasing ocean temperature, acidification and pollution. In many regions, ecosystems are already severely deteriorating and are further threatened by increasing population pressure and large coastal development projects. Degradation of these marine habitats will lead to environmental costs, as well as significant economic losses. Therefore, it will result in a missed opportunity for the bordering countries to develop a sustainable blue economy and integrate innovative nature-based solutions. Recognizing that securing the Red Sea ecosystems’ future must occur in synergy with continued social and economic growth, we developed an action plan for the conservation, restoration, and growth of marine environments of the Red Sea. We then investigated the level of resources for financial and economic investment that may incentivize these activities. This study presents a set of commercially viable financial investment strategies, ecological innovations, and sustainable development opportunities, which can, if implemented strategically, help ensure long-term economic benefits while promoting environmental conservation. We make a case for investing in blue natural capital and propose a strategic development model that relies on maintaining the health of natural ecosystems to s

Corals house a variety of microorganisms which they depend on for their survival, including endosymbiotic dinoflagellates (Symbiodiniaceae) and bacteria. While cnidarian-microorganism interactions are widely studied, Symbiodiniaceae-bacteria interactions are only just beginning to receive attention. Here, we describe the localization and composition of the bacterial communities associated with cultures of 11 Symbiodiniaceae strains from nine species and six genera. Three-dimensional confocal laser scanning and electron microscopy revealed bacteria are present inside the Symbiodiniaceae cells as well as closely associated with their external cell surface. Bacterial pure cultures and 16S rRNA gene metabarcoding from Symbiodiniaceae cultures highlighted distinct and highly diverse bacterial communities occur intracellularly, closely associated with the Symbiodiniaceae outer cell surface and loosely associated (i.e., in the surrounding culture media). The intracellular bacteria are highly conserved across Symbiodiniaceae species, suggesting they may be involved in Symbiodiniaceae physiology. Our findings provide unique new insights into the biology of Symbiodiniaceae.

Coral reef restoration is a rapidly growing movement galvanized by the accelerating degradation of the world's tropical coral reefs. The need for concerted and collaborative action focused on the recovery of coral reef ecosystems coalesced in the creation of the Coral Restoration Consortium (CRC) in 2017. In March 2020, the CRC leadership team met for a biennial review of international coral reef restoration efforts and a discussion of perceived knowledge and implementation bottlenecks that may impair scalability and efficacy. Herein we present six priorities wherein the CRC will foster scientific advancement and collaboration to: (1) increase restoration efficiency, focusing on scale and cost-effectiveness of deployment; (2) scale up larval-based coral restoration efforts, emphasizing recruit health, growth, and survival; (3) ensure restoration of threatened coral species proceeds within a population-genetics management context; (4) support a holistic approach to coral reef ecosystem restoration; (5) develop and promote the use of standardized terms and metrics for coral reef restoration; and (6) support coral reef restoration practitioners working in diverse geographic locations. These priorities are not exhaustive nor do we imply that accomplishing these tasks alone will be sufficient to restore coral reefs globally; rather these are topics where we feel the CRC community of practice can make timely and significant contributions to facilitate the growth of coral reef restoration as a practical conservation strategy. The goal for these collective actions is to provide tangible, local-scale advancements in reef condition that offset declines resulting from local and global stressors including climate change.

We employed Fast Repetition Rate fluorometry for high-resolution mapping of marine phytoplankton photophysiology and primary photochemistry in the Lancaster Sound and Barrow Strait regions of the Canadian Arctic Archipelago in the summer of 2019. Continuous ship-board analysis of chlorophyll a variable fluorescence demonstrated relatively low photochemical efficiency over most of the cruise-track, with the exception of localized regions within Barrow Strait, where there was increased vertical mixing and proximity to land-based nutrient sources. Along the full transect, we observed strong non-photochemical quenching of chlorophyll fluorescence, with relaxation times longer than the 5-minute period used for dark acclimation. Such long-term quenching effects complicate continuous underway acquisition of fluorescence amplitude-based estimates of photosynthetic electron transport rates, which rely on dark acclimation of samples. As an alternative, we employed a new algorithm to derive electron transport rates based on analysis of fluorescence relaxation kinetics, which does not require dark acclimation. Direct comparison of kinetics- and amplitude-based electron transport rate measurements demonstrated that kinetic-based estimates were, on average, 2-fold higher than amplitude-based values. The magnitude of decoupling between the two electron transport rate estimates increased in association with photophysiological diagnostics of nutrient stress. Discrepancies between electron transport rate estimates likely resulted from the use of different photophysiological parameters to derive the kinetics- and amplitude-based algorithms, and choice of numerical model used to fit variable fluorescence curves and analyze fluorescence kinetics under actinic light. Our results highlight environmental and methodological influences on fluorescence-based photochemistry estimates, and prompt discussion of best-practices for future underway fluorescence-based efforts to monitor phytoplankto

Marine diazotrophs are a diverse group with key roles in biogeochemical fluxes linked to primary productivity. The unicellular, diazotrophic cyanobacterium Cyanothece is widely found in coastal, subtropical oceans. We analyze the consequences of diazotrophy on growth efficiency, compared to NO3–-supported growth in Cyanothece, to understand how cells cope with N2-fixation when they also have to face carbon limitation, which may transiently affect populations in coastal environments or during blooms of phytoplankton communities. When grown in obligate diazotrophy, cells face the double burden of a more ATP-demanding N-acquisition mode and additional metabolic losses imposed by the transient storage of reducing potential as carbohydrate, compared to a hypothetical N2 assimilation directly driven by photosynthetic electron transport. Further, this energetic burden imposed by N2-fixation could not be alleviated, despite the high irradiance level within the cultures, because photosynthesis was limited by the availability of dissolved inorganic carbon (DIC), and possibly by a constrained capacity for carbon storage. DIC limitation exacerbates the costs on growth imposed by nitrogen fixation. Therefore, the competitive efficiency of diazotrophs could be hindered in areas with insufficient renewal of dissolved gases and/or with intense phytoplankton biomass that both decrease available light energy and draw the DIC level down.