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Sometimes called the “lab rat” of coral research, Stylophora pistillata (Esper, 1797) has been extensively used in coral biology in studies ranging from reef ecology to coral metabolic processes, and has been used as a model for investigations into molecular and cellular biology. Previously thought to be a common species spanning a wide distribution through the Indo-Pacific region, “S. pistillata” is in fact four genetically distinct lineages (clades) with different evolutionary histories and geographical distributions. Here, we review the studies of stress responses of S. pistillata sensu lato (clades 1–4) and highlight research trends and knowledge gaps. We identify 126 studies on stress responses including effects of temperature, acidification, eutrophication, pollutants and other local impacts. We find that most studies have focused on the effect of single stressors, especially increased temperature, and have neglected the combined effects of multiple stressors. Roughly 61% of studies on S. pistillata come from the northern Red Sea (clade 4), at the extreme limit of its current distribution; clades 2 and 3 are virtually unstudied. The overwhelming majority of studies were conducted in laboratory or mesocosm conditions, with field experiments constituting only 2% of studies. We also note that a variety of experimental designs and treatment conditions makes it difficult to draw general conclusions about the effects of particular stressors on S. pistillata. Given those knowledge gaps and limitations in the published research, we suggest a more standardized approach to compare responses across geographically disparate populations and more accurately anticipate responses to predicted future climate conditions., SI

Aquaculture production has increased steadily in many tropical countries over the past few decades, although impact assessments have been frequently neglected. We investigated the impacts of an offshore barramundi fish farm on water quality in the southern-central Red Sea, a traditionally understudied tropical, oligotrophic, and semi-enclosed basin. Inorganic nutrients, particulate matter, chlorophyll-a, and heterotrophic bacteria were measured periodically over 8 months around the farm. Water down-current from the farm had, on average, more heterotrophic bacteria and chlorophyll-a than up-current (11% and 34% higher, respectively). Ratios of dissolved inorganic nitrogen:phosphorus down-current from the farm were lower than ratios up-current (mean 9.8 vs 16.0, respectively). Phosphate, inorganic nitrogen, and particulate matter showed patterns of enrichment associated with the farm after a fish feeding event. Strategies such as feed optimization and considering hydrodynamics in site selection may improve water quality for future fish farms in Saudi Arabia and other tropical countries., SI

The bathypelagic ocean (1000-4000 m depth) is the largest aquatic biome on Earth but it is still largely unexplored. Due to its prevalent low dissolved organic carbon concentrations, most of the prokaryotic metabolic activity is assumed to be associated to particles. The role of free-living prokaryotes has thus been mostly ignored, except that of some chemolithoautotrophic lineages. Here we used a global bathypelagic survey of size-fractionated metagenomic and 16S (genes and transcripts) data and performed a differential abundance analysis to explore the functional traits of the different prokaryotic life-strategies, their contribution to the active microbiome, and the role that the quality of the dissolved organic matter (DOM) plays in driving this contribution. We found that free-living prokaryotes have limited capacity to uplift their metabolism in response to environmental changes and display comparatively lower growth rates than particle associated prokaryotes, but are responsible for the synthesis of vitamins in the bathypelagic. Furthermore, their contribution to the active prokaryotic microbiome increased towards waters depleted of labile DOM, which represented a large fraction of the tropical and subtropical ocean sampled stations. This points to a relevant yet overlooked role of free-living prokaryotes in DOM cycling in the vast bathypelagic desert.

Ecosystem services provided by coral reefs may be susceptible to the combined effects of benthic species shifts and anthropogenic nutrient pollution, but related field studies are scarce. We thus investigated in situ how dissolved inorganic nutrient enrichment, maintained for two months, affected community-wide biogeochemical functions of intact coral- and degraded algae-dominated reef patches in the central Red Sea. Results from benthic chamber incubations revealed 87% increased gross productivity and a shift from net calcification to dissolution in algae-dominated communities after nutrient enrichment, but the same processes were unaffected by nutrients in neighboring coral communities. Both community types changed from net dissolved organic nitrogen sinks to sources, but the increase in net release was 56% higher in algae-dominated communities. Nutrient pollution may, thus, amplify the effects of community shifts on key ecosystem services of coral reefs, possibly leading to a loss of structurally complex habitats with carbonate dissolution and altered nutrient recycling.

In coral reefs, dissolved organic matter (DOM) cycling is a critical process for sustaining ecosystem functioning. However, global and local stressors have caused persistent shifts from coral- to algae-dominated benthic communities. The influence of such phase shifts on DOM nature and its utilization by heterotrophic bacterioplankton remains poorly studied. Every second month for one year, we retrieved seawater samples enriched in DOM produced by coral- and algae-dominated benthic communities in a central Red Sea reef during a full annual cycle. Seawater incubations were conducted in the laboratory under in situ temperature and light conditions by inoculating enriched DOM samples with bacterial assemblages collected in the surrounding waters. Dissolved organic carbon (DOC) concentrations were higher in the warmer months (May-September) in both communities, resulting in higher specific growth rates and bacterial growth efficiencies (BGE). However, these high summer values were significantly enhanced in algal-DOM relative to coral-DOM, suggesting the potential for bacterioplankton biomass increase in reefs with algae replacing healthy coral cover under warmer conditions. The potential exacerbation of heterotrophic bacterial activity in the ongoing widespread regime shift from coral- to algae-dominated communities may have detrimental consequences for the overall health of tropical coral reefs. (C) 2020 The Authors. Published by Elsevier B.V.

The diel variability of the abundance and cell size of picoplanktonic groups in the central Red Sea was monitored every 2 h in situ on 4 occasions (once per season) from 2015 to 2016. We distinguished Prochlorococcus, low (LF-Syn) and high (HF-Syn) fluorescence Synechococcus, small (Speuk) and large (Lpeuk) picoeukaryotes and two groups of heterotrophic prokaryotes of low (LNA) and high (HNA) nucleic acid content. The diel variability in abundance was less marked than in cell size and more apparent in autotrophs than heterotrophs. Specific growth rates were estimated by an empirical relationship from measurements obtained in bottle incubations of surface and deep samples collected in the winter compared with in situ variations in cell size over 24 h. Autotrophic picoplankton groups generally grew faster (0.23–0.77 d–1) than heterotrophic prokaryotes (0.12–0.50 d–1). Surface to 100 m depth-weighted specific growth rates displayed a clear seasonal pattern for Prochlorococcus, with maxima in winter (0.77 ± 0.07 d–1) and minima in fall (0.52 ± 0.07 d–1). The two groups of Synechococcus peaked in spring, with slightly higher growth rates of LF-Syn (0.57 ± 0.04 d–1) than HF-Syn (0.43 ± 0.04 d–1). Speuk and Lpeuk showed different seasonal patterns, with lower values of the former (0.27 ± 0.02 and 0.37 ± 0.04 d–1, respectively). HNA consistently outgrew LNA heterotrophic prokaryotes, with a higher growth in the epipelagic (0–200 m, 0.36 ± 0.03 d–1) than in the mesopelagic (200–700 m, 0.26 ± 0.03 d–1), while no differences were found for LNA cells (0.19 ± 0.03 d–1 and 0.17 ± 0.02 d–1, respectively). With all data pooled, the mean diel abundances of autotrophic picoplankton in the upper epipelagic and of HNA cells in the epipelagic and mesopelagic layers were significantly correlated with the specific growth rates estimated from cell size variations. Our high-resolution sampling dataset suggests that changes in growth rates underlie the noticeable seasonality of picoplankton recently described in these tropical waters.

Special issue on Oxygen Minimum Zone Microbiology.-- 11 pages, 5 figures, 3 tables, supporting information https://doi.org/10.1111/1462-2920.15504.-- This is the pre-peer reviewed version of the following article: Yaiza M. Castillo, Irene Forn, Sheree Yau, Xosé Anxelu G. Morán, Laura Alonso-Sáez, Néstor Arandia-Gorostidi, Dolors Vaqué, Marta Sebastián; Seasonal dynamics of natural Ostreococcus viral infection at the single cell level using VirusFISH; Environmental Microbiology 23(6): 3009-3019 (2021), which has been published in final form at https://doi.org/10.1111/1462-2920.15504. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions, Ostreococcus is a cosmopolitan marine genus of phytoplankton found in mesotrophic and oligotrophic waters, and the smallest free-living eukaryotes known to date, with a cell diameter close to 1 μm. Ostreococcus has been extensively studied as a model system to investigate viral–host dynamics in culture, yet the impact of viruses in naturally occurring populations is largely unknown. Here, we used Virus Fluorescence in situ Hybridization (VirusFISH) to visualize and quantify viral-host dynamics in natural populations of Ostreococcus during a seasonal cycle in the central Cantabrian Sea (Southern Bay of Biscay). Ostreococcus were predominantly found during summer and autumn at surface and 50 m depth, in coastal, mid-shelf and shelf waters, representing up to 21% of the picoeukaryotic communities. Viral infection was only detected in surface waters, and its impact was variable but highest from May to July and November to December, when up to half of the population was infected. Metatranscriptomic data available from the mid-shelf station unveiled that the Ostreococcus population was dominated by the species O. lucimarinus. This work represents a proof of concept that the VirusFISH technique can be used to quantify the impact of viruses on targeted populations of key microbes from complex natural communities, This work was supported by the Spanish projects MEFISTO (CTM2013-43767-P, MINECO) and ALLFLAGS (CTM2016-75083-R, MINECO). YMC was supported by a FPI Spanish fellowship (BES-2014-067849), SY was supported by a Juan de la Cierva fellowship (IJCI-2017-34245) and LAS was supported by a Juan de la Cierva and Ramon y Cajal contract (RYC-2012-11404). MS was supported by a Viera y Clavijo contract funded by the ACIISI and the ULPGC. NAG was supported by Basque Government's PhD-program fellowship, With the funding support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI)

This is the data to "High summer temperatures amplify functional differences between coral- and algae-dominated reef communities". All information on how the dataset was collected can be found in the manuscript. Abstract of the manuscript: Shifts from coral to algal dominance are expected to increase in tropical coral reefs as a result of anthropogenic disturbances. The consequences for key ecosystem functions such as primary productivity, calcification, and nutrient recycling are poorly understood, particularly under changing environmental conditions. We used a novel in situ incubation approach to compare functions of coral- and algae-dominated communities in the central Red Sea bi-monthly over an entire year. In situ gross and net community primary productivity, calcification, dissolved organic carbon fluxes, dissolved inorganic nitrogen fluxes, and their respective activation energies were quantified to describe the effects of seasonal changes. Overall, coral-dominated communities exhibited 30% lower net productivity and 10 times higher calcification than algae-dominated communities. Estimated activation energies indicated a higher thermal sensitivity of coral-dominated communities. In these communities, net productivity and calcification were negatively correlated with temperature (>40% and >65% reduction, respectively, with +5°C increase from winter to summer), while carbon losses via respiration and dissolved organic carbon release were more than doubled at higher temperatures. In contrast, algae-dominated communities doubled net productivity in summer, while calcification and dissolved organic carbon fluxes were unaffected. These results suggest pronounced changes in community functioning associated with phase shifts. Algae-dominated communities may outcompete coral-dominated communities due to their higher productivity and carbon retention to support fast biomass accumulation while compromising the formation of important reef framework structures. Higher temperatures likely amplify these functional differences, indicating a high vulnerability of ecosystem functions of coral-dominated communities to temperatures even below coral bleaching thresholds. Our results suggest that ocean warming may not only cause but also amplify coral-algal phase shifts in coral reefs. Usage information: The data Excel file contains two data sheets: Sheet 1 (Community composition): This sheet gives the community composition of the assessed benthic communities in % cover of functional groups. Sheet 2 (Metabolism): This sheet contains the metabolic data of the benthic communities. All abbreviations and units are in the related publication.

Interactions between autotrophic and heterotrophic bacteria are fundamental for marine biogeochemical cycling. How global warming will affect the dynamics of these essential microbial players is not fully understood. The aims of this study were to identify the major groups of heterotrophic bacteria present in a Synechococcus culture originally isolated from the Red Sea and assess their joint responses to experimental warming within the metabolic ecology framework. A co-culture of Synechococcus sp. RS9907 and their associated heterotrophic bacteria, after determining their taxonomic affiliation by 16S rRNA gene sequencing, was acclimated and maintained in the lab at different temperatures (24–34°C). The abundance and cellular properties of Synechococcus and the three dominant heterotrophic bacterial groups (pertaining to the genera Paracoccus, Marinobacter, and Muricauda) were monitored by flow cytometry. The activation energy of Synechococcus, which grew at 0.94–1.38 d–1, was very similar (0.34 ± 0.02 eV) to the value hypothesized by the metabolic theory of ecology (MTE) for autotrophs (0.32 eV), while the values of the three heterotrophic bacteria ranged from 0.16 to 1.15 eV and were negatively correlated with their corresponding specific growth rates (2.38–24.4 d–1). The corresponding carrying capacities did not always follow the inverse relationship with temperature predicted by MTE, nor did we observe a consistent response of bacterial cell size and temperature. Our results show that the responses to future ocean warming of autotrophic and heterotrophic bacteria in microbial consortia might not be well described by theoretical universal rules.

We would like to thank Nora Gutierrez Avello (13), Maria de Lluch Calleja Serra (15), as well as the young reviewers and their mentor who read the original draft and provided very helpful feedback to improve it and make it understandable for their age range.

Research was supported by KAUST and by U.S. NSF grant OCE-1558580 to J.R.P. M.K.W. would like to thank colleagues in the Reef Ecology Lab and Luis Silva, Snjezana Ivetic, Najwa Al-Otaibi, and Maria Ll. Calleja for their help with data analyses.

Recent work suggests that temperature effects on marine heterotrophic bacteria are strongly seasonal, but few attempts have been made to concurrently assess them across trophic levels. Here, we estimated the temperature sensitivities (using activation energies, E) of autotrophic and heterotrophic microbial plankton net growth rates over an annual cycle in NE Atlantic coastal waters. Phytoplankton grew in winter and late autumn (0.41 ± 0.16 SE d-1 ) and decayed in the remaining months (-0.42 ± 0.10 d-1 ). Heterotrophic microbes shared a similar seasonality, with positive net growth for bacteria (0.14-1.48 d-1 ), while nanoflagellates had higher values (> 0.4 d-1 ) in winter and spring relative to the rest of the year (-0.46 to 0.29 d-1 ). Net growth rates activation energies showed similar dynamics in the three groups (-1.07 to 1.51 eV), characterized by maxima in winter, minima in summer and resumed increases in autumn. Microbial plankton E values were significantly correlated with nitrate concentrations as a proxy for nutrient availability. Nutrient-sufficiency (i.e., > 1 μmol l-1 nitrate) resulted in significantly higher activation energies of phytoplankton and heterotrophic nanoflagellates relative to nutrient-limited conditions. We suggest that only within spatio-temporal windows of both moderate bottom-up and top-down controls will temperature have a major enhancing effect on microbial growth.

The ecological status of an ecosystem can be approached by the taxa present but also by the size of individual organisms. In aquatic ecosystems, flow cytometry (FC) allows to study the individual size spectra and broad community composition through the evaluation of cytometric categories. The Red Sea represents a warm oligotrophic environment with a strong diel signal of vertically migrating mesopelagic fish, which feed at night at the surface and release dissolved organic carbon (DOC) at depth during day-time. However, knowledge about how these conditions affect the dynamics of heterotrophic prokaryotes (HP) and their coupling with DOC is lacking. Here, we analyzed a high frequency sampling over 24 h to identify the community structure and compositional changes of HP in the epipelagic and mesopelagic layers of the central Red Sea. Our results show marked vertical and diel changes in HP communities in both layers. Specifically, the relative contribution of high nucleic acid content cells was remarkably linked to changes in DOC concentration and properties. The patterns observed were likely associated to the diel vertical migration of mesopelagic fish. These findings reveal that the structure of microbial communities in warm oligotrophic environments may be more dynamic than previously thought.

Although temperature is a key driver of bacterioplankton metabolism, the effect of ocean warming on different bacterial phylogenetic groups remains unclear. Here, we conducted monthly short-term incubations with natural coastal bacterial communities over an annual cycle to test the effect of experimental temperature on the growth rates and carrying capacities of four phylogenetic groups: SAR11, Rhodobacteraceae, Gammaproteobacteria and Bacteroidetes. SAR11 was the most abundant group year-round as analysed by CARD-FISH, with maximum abundances in summer, while the other taxa peaked in spring. All groups, including SAR11, showed high temperature-sensitivity of growth rates and/or carrying capacities in spring, under phytoplankton bloom or post-bloom conditions. In that season, Rhodobacteraceae showed the strongest temperature response in growth rates, estimated here as activation energy (E, 1.43 eV), suggesting an advantage to outcompete other groups under warmer conditions. In summer E values were in general lower than 0.65 eV, the value predicted by the Metabolic Theory of Ecology (MTE). Contrary to MTE predictions, carrying capacity tended to increase with warming for all bacterial groups. Our analysis confirms that resource availability is key when addressing the temperature response of heterotrophic bacterioplankton. We further show that even under nutrient-sufficient conditions, warming differentially affected distinct bacterioplankton taxa.

Here we assess the temperature dependence of the metabolic rates (gross primary production - GPP, community respiration - CR and the ratio GPP/CR) of oceanic plankton communities. We compile data from 133 stations of the Malaspina 2010 Expedition, distributed among the subtropical and tropical Atlantic, Pacific and Indian oceans. We used the in vitro technique to measured metabolic rates during 24 h incubations at three different sampled depths: surface, 20% and 1% of the photosynthetically active radiation measured at surface. We also measured the % of ultraviolet B radiation (UVB) penetrating at surface waters. GPP and CR rates increased with warming, albeit different responses were observed for each sampled depth. The overall GPP/CR ratio declined with warming. Higher activation energies (Ea´s) were derived for both processes (GPPChla = 0.97; CRChla = 1.26; CRHPA= 0.95 eV) compared to those previously reported. The Indian Ocean showed the highest Ea (GPPChla = 1.70; CRChla = 1.48; CRHPA= 0.57 eV), while the Atlantic Ocean showed the lowest (GPPChla = 0.86; CRChla = 0.77; CRHPA= -0.13 eV). We believe that the difference between previous assessments and the ones presented here can be explained by the overrepresentation of Atlantic communities in the previous data sets. We found that UVB radiation also affects the temperature dependence of surface GPP, which decreased rather than increased under high levels of UVB. Ocean warming, which causes stratification and oligotrophication of the subtropical and tropical oceans, may lead to reduced surface GPP as a result of increased penetration of UVB radiation.

Bacterioplankton play a pivotal role in marine ecosystems. However, their temporal dynamics and underlying control mechanisms are poorly understood in tropical regions such as the Red Sea. Here, we assessed the impact of bottom-up (resource availability) and top-down (viruses and heterotrophic nanoflagellates) controls on bacterioplankton abundances by weekly sampling a coastal central Red Sea site in 2017. We monitored microbial abundances by flow cytometry together with a set of environmental variables including temperature, salinity, dissolved organic and inorganic nutrients and chlorophyll a. We distinguished five groups of heterotrophic bacteria depending on their physiological properties relative nucleic acid content, membrane integrity and cell-specific respiratory activity, two groups of Synechococcus cyanobacteria and three groups of viruses. Viruses controlled heterotrophic bacteria for most of the year, as supported by a negative correlation between their respective abundances and a positive one between bacterial mortality rates and mean viral abundances. On the contrary, heterotrophic nanoflagellates abundance covaried with that of heterotrophic bacteria. Heterotrophic nanoflagellates showed preference for larger bacteria from both the high and low nucleic acid content groups. Our results demonstrate that top-down control is fundamental in keeping heterotrophic bacterioplankton abundances low (< 5 × 10 5 cells mL−1) in Red Sea coastal waters., The weekly variations of bacterioplankton standing stocks in the central Red Sea coastal water are apparently controlled by top-down regulators (viruses and heterotrophic nanoflagellates).