Too hot to handle? An urgent need to understand climate change impacts on the biogeochemistry of tropical coastal waters.

Tropical regions contain ecologically and socio-economically important habitats, and are home to about 3.8 billion people, many of which directly depend on tropical coastal waters for their well-being. At the basis of these ecosystems are biogeochemical processes. Climate change is expected to have a greater impact in the tropics compared to temperate regions because of the relatively stable environmental conditions found there. However, it was surprising to find only 660 research articles published focusing on the impact of climate change on the biogeochemistry of coastal tropical waters compared to 4823 for temperate waters. In this perspective, we highlight important topics in need of further research. Specifically, we suggest that in tropical regions compared to temperate counterparts climate change stressors will be experienced differently, that organisms have a lower acclimation capacity, and that long-term baseline biogeochemical datasets useful for quantifying future changes are lacking. The low number of research papers on the impacts of climate change in coastal tropical regions is likely due to a mix of reasons including limited resources for research and limited number of long time series in many developing tropical countries. Finally, we propose some action points that we hope will stimulate more studies in tropical coastal waters.

Spatial and seasonal variability of picoplankton abundance and growth rates in the southern Bay of Biscay.

Autotrophic and heterotrophic picoplankton play fundamental roles in marine food webs and biogeochemical cycles. However, their growth responses have seldom been jointly assessed, including many temperate regions such as the Bay of Biscay. There, previous studies have shown their relevance in carbon fluxes. We describe here the spatio-temporal variability of the abundances and growth rates of the picoplanktonic groups routinely distinguished by flow cytometry (Synechococcus and Prochlorococcus cyanobacteria, two groups of differently sized picoeukaryotes and two groups of heterotrophic bacteria distinguished by their relative nucleic acid content) in the central Cantabrian Sea (S Bay of Biscay). To that end, from February to December 2021 we collected surface water on 5 occasions from 6 stations distributed along the S Bay of Biscay (6-3°W) and incubated it after removing protistan grazers in order to determine their dynamics along the seasonal cycle as well as the inshore-offshore and the west-east gradients. Seasonal variations in initial and maximum abundances generally matched previous knowledge of the region but growth rates were more variable, with Prochlorococcus and high nucleic acid (HNA) bacteria showing the maximum values (up to 2 d-1) while negative growth was observed in one third of Synechococcus incubations. Temporal differences generally overrode differences along the inshore-offshore gradient in trophic status while in situ and maximum abundances of most of the groups generally decreased towards the east following the increase in stratification and lower nutrient availability. Responses to stratification suggest Prochlorococcus and low nucleic acid (LNA) cells may prevail among autotrophic and heterotrophic bacteria, respectively, in a warmer ocean.

Predicting Anaerobic Membrane Bioreactor Performance Using Flow-Cytometry-Derived High and Low Nucleic Acid Content Cells.

Having a tool to monitor the microbial abundances rapidly and to utilize the data to predict the reactor performance would facilitate the operation of an anaerobic membrane bioreactor (AnMBR). This study aims to achieve the aforementioned scenario by developing a linear regression model that incorporates a time-lagging mode. The model uses low nucleic acid (LNA) cell numbers and the ratio of high nucleic acid (HNA) to LNA cells as an input data set. First, the model was trained using data sets obtained from a 35 L pilot-scale AnMBR. The model was able to predict the chemical oxygen demand (COD) removal efficiency and methane production 3.5 days in advance. Subsequent validation of the model using flow cytometry (FCM)-derived data (at time t - 3.5 days) obtained from another biologically independent reactor did not exhibit any substantial difference between predicted and actual measurements of reactor performance at time t. Further cell sorting, 16S rRNA gene sequencing, and correlation analysis partly attributed this accurate prediction to HNA genera (e.g., Anaerovibrio and unclassified Bacteroidales) and LNA genera (e.g., Achromobacter, Ochrobactrum, and unclassified Anaerolineae). In summary, our findings suggest that HNA and LNA cell routine enumeration, along with the trained model, can derive a fast approach to predict the AnMBR performance.

Increased prokaryotic diversity in the Red Sea deep scattering layer.

BACKGROUND: The diel vertical migration (DVM) of fish provides an active transport of labile dissolved organic matter (DOM) to the deep ocean, fueling the metabolism of heterotrophic bacteria and archaea. We studied the impact of DVM on the mesopelagic prokaryotic diversity of the Red Sea focusing on the mesopelagic deep scattering layer (DSL) between 450-600 m. RESULTS: Despite the general consensus of homogeneous conditions in the mesopelagic layer, we observed variability in physico-chemical variables (oxygen, inorganic nutrients, DOC) in the depth profiles. We also identified distinct seasonal indicator prokaryotes inhabiting the DSL, representing between 2% (in spring) to over 10% (in winter) of total 16S rRNA gene sequences. The dominant indicator groups were Alteromonadales in winter, Vibrionales in spring and Microtrichales in summer. Using multidimensional scaling analysis, the DSL samples showed divergence from the surrounding mesopelagic layers and were distributed according to depth (47% of variance explained). We identified the sources of diversity that contribute to the DSL by analyzing the detailed profiles of spring, where 3 depths were sampled in the mesopelagic. On average, 7% was related to the epipelagic, 34% was common among the other mesopelagic waters and 38% was attributable to the DSL, with 21% of species being unique to this layer. CONCLUSIONS: We conclude that the mesopelagic physico-chemical properties shape a rather uniform prokaryotic community, but that the 200 m deep DSL contributes uniquely and in a high proportion to the diversity of the Red Sea mesopelagic.

Global biogeography of the smallest plankton across ocean depths.

Tiny ocean plankton (picoplankton) are fundamental for the functioning of the biosphere, but the ecological mechanisms shaping their biogeography were partially understood. Comprehending whether these microorganisms are structured by niche versus neutral processes is relevant in the context of global change. We investigate the ecological processes (selection, dispersal, and drift) structuring global-ocean picoplanktonic communities inhabiting the epipelagic (0 to 200 meters), mesopelagic (200 to 1000 meters), and bathypelagic (1000 to 4000 meters) zones. We found that selection decreased, while dispersal limitation increased with depth, possibly due to differences in habitat heterogeneity and dispersal barriers such as water masses and bottom topography. Picoplankton ß-diversity positively correlated with environmental heterogeneity and water mass variability, but this relationship tended to be weaker for eukaryotes than for prokaryotes. Community patterns were more pronounced in the Mediterranean Sea, probably because of its cross-basin environmental heterogeneity and deep-water isolation. We conclude that different combinations of ecological mechanisms shape the biogeography of the ocean microbiome across depths.

Seasonality of top-down control of bacterioplankton at two central Red Sea sites with different trophic status.

The role of bottom-up (nutrient availability) and top-down (grazers and viruses mortality) controls on tropical bacterioplankton have been rarely investigated simultaneously from a seasonal perspective. We have assessed them through monthly samplings over 2 years in inshore and offshore waters of the central Red Sea differing in trophic status. Flow cytometric analysis allowed us to distinguish five groups of heterotrophic bacteria based on physiological properties (nucleic acid content, membrane integrity and active respiration), three groups of cyanobacteria (two populations of Synechococcus and Prochlorococcus), heterotrophic nanoflagellates (HNFs) and three groups of viruses based on nucleic acid content. The dynamics of bacterioplankton and their top-down controls varied with season and location, being more pronounced in inshore waters. HNFs abundances showed a strong preference for larger prey inshore (r = -0.62 to -0.59, p = 0.001-0.002). Positive relationships between viruses and heterotrophic bacterioplankton abundances were more marked inshore (r = 0.67, p < 0.001) than offshore (r = 0.44, p = 0.03). The negative correlation between HNFs and viruses abundances (r = -0.47, p = 0.02) in shallow waters indicates a persistent seasonal switch between protistan grazing and viral lysis that maintains the low bacterioplankton stocks in the central Red Sea area.

Growth dynamics and transcriptional responses of a Red Sea Prochlorococcus strain to varying temperatures.

Prochlorococcus play a crucial role in the ocean's biogeochemical cycling, but it remains controversial how they will respond to global warming. Here we assessed the response to temperature (22-30°C) of the growth dynamics and gene expression profiles of a Red Sea Prochlorococcus strain (RSP50) in a non-axenic culture. Both the specific growth rate (0.55-0.80 day-1 ) and cell size (0.04-0.07 µm3 ) of Prochlorococcus increased significantly with temperature. The primary production released extracellularly ranged from 20% to 34%, with humic-like fluorescent compounds increasing up to fivefold as Prochlorococcus reached its maximum abundance. At 30°C, genes involved in carbon fixation such as CsoS2 and CsoS3 and photosynthetic electron transport including PTOX were downregulated, suggesting a cellular homeostasis and energy saving mechanism response. In contrast, PTOX was found upregulated at 22°C and 24°C. Similar results were found for transaldolase, related to carbon metabolism, and citrate synthase, an important enzyme in the TCA cycle. Our data suggest that in spite of the currently warm temperatures of the Red Sea, Prochlorococcus can modulate its gene expression profiles to permit growth at temperatures lower than its optimum temperature (28°C) but is unable to cope with temperatures exceeding 30°C.

Temperature enhances the functional diversity of dissolved organic matter utilization by coastal marine bacteria.

Although bulk bacterial metabolism in response to temperature has been determined for different oceanic regions, the impact of temperature on the functional diversity of dissolved organic matter (DOM) utilization has been largely unexplored. Here, we hypothesized that besides modifying the rates of carbon utilization, temperature can also alter the diversity of substrates utilized. The patterns of utilization of 31 model DOM compounds (as represented in Biolog EcoPlate™) by bacterioplankton were assessed using inocula from surface waters of the southern Bay of Biscay continental shelf over 1 year. Bacteria utilized more polymers and carbohydrates in late spring and summer than in winter, likely reflecting changes in substrate availability linked to the release and accumulation of DOM in phytoplankton post-bloom conditions. Seawater temperature correlated positively with the number of substrates utilized (i.e. functional richness) and this relationship was maintained in monthly experimental incubations spanning 3°C below and above in situ values. The enhancement of functional richness with experimental warming displayed a unimodal response to ambient temperature, peaking at 16°C. This temperature acted as a threshold separating nutrient-sufficient from nutrient-deficient conditions at the study site, suggesting that trophic conditions will be critical in the response of microbial DOM utilization to future warming.

High-Frequency Variability of Bacterioplankton in Response to Environmental Drivers in Red Sea Coastal Waters.

Autotrophic and heterotrophic bacterioplankton are essential to the biogeochemistry of tropical ecosystems. However, the processes that govern their dynamics are not well known. We provide here a high-frequency assessment of bacterial community dynamics and concurrent environmental factors in Red Sea coastal waters. Weekly sampling of surface samples during a full annual cycle at an enclosed station revealed high variability in ecological conditions, which reflected in changes of major bacterioplankton communities. Temperature varied between 23 and 34°C during the sampling period. Autotrophic (Synechococcus, 1.7-16.2 × 104 cells mL-1) and heterotrophic bacteria (1.6-4.3 × 105 cells mL-1) showed two maxima in abundance in spring and summer, while minima were found in winter and autumn. Heterotrophic cells with high nucleic acid content (HNA) peaked in July, but their contribution to the total cell counts (35-60%) did not show a clear seasonal pattern. Actively respiring cells (CTC+) contributed between 4 and 51% of the total number of heterotrophic bacteria, while live cells (with intact membrane) consistently accounted for over 90%. Sequenced 16S rRNA amplicons revealed a predominance of Proteobacteria in summer and autumn (>40%) and a smaller contribution in winter (21-24%), with members of the Alphaproteobacteria class dominating throughout the year. The contribution of the Flavobacteriaceae family was highest in winter (21%), while the Rhodobacteraceae contribution was lowest (6%). Temperature, chlorophyll-a, and dissolved organic carbon concentration were the environmental variables with the greatest effects on bacterial abundance and diversity patterns.

Diel dynamics of dissolved organic matter and heterotrophic prokaryotes reveal enhanced growth at the ocean's mesopelagic fish layer during daytime.

Contrary to epipelagic waters, where biogeochemical processes closely follow the light and dark periods, little is known about diel cycles in the ocean's mesopelagic realm. Here, we monitored the dynamics of dissolved organic matter (DOM) and planktonic heterotrophic prokaryotes every 2 h for one day at 0 and 550 m (a depth occupied by vertically migrating fishes during light hours) in oligotrophic waters of the central Red Sea. We additionally performed predator-free seawater incubations of samples collected from the same site both at midnight and at noon. Comparable in situ variability in microbial biomass and dissolved organic carbon concentration suggests a diel supply of fresh DOM in both layers. The presence of fishes in the mesopelagic zone during daytime likely promoted a sustained, longer growth of larger prokaryotic cells. The specific growth rates were consistently higher in the noon experiments from both depths (surface: 0.34 vs. 0.18 d-1, mesopelagic: 0.16 vs. 0.09 d-1). Heterotrophic prokaryotes in the mesopelagic layer were also more efficient at converting extant DOM into new biomass. These results suggest that the ocean's twilight zone receives a consistent diurnal supply of labile DOM from the diel vertical migration of fishes, enabling an unexpectedly active community of heterotrophic prokaryotes.

Stylophora under stress: A review of research trends and impacts of stressors on a model coral species.

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. pistillatasensulato (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.

Localized effects of offshore aquaculture on water quality in a tropical sea.

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.

Temperature Responses of Heterotrophic Bacteria in Co-culture With a Red Sea Synechococcus Strain.

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.

Nutrient pollution enhances productivity and framework dissolution in algae- but not in coral-dominated reef communities.

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.

Seasonal dynamics of natural Ostreococcus viral infection at the single cell level using VirusFISH.

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.

Fine-scale metabolic discontinuity in a stratified prokaryote microbiome of a Red Sea deep halocline.

Deep-sea hypersaline anoxic basins are polyextreme environments in the ocean's interior characterized by the high density of brines that prevents mixing with the overlaying seawater, generating sharp chemoclines and redoxclines up to tens of meters thick that host a high concentration of microbial communities. Yet, a fundamental understanding of how such pycnoclines shape microbial life and the associated biogeochemical processes at a fine scale, remains elusive. Here, we applied high-precision sampling of the brine-seawater transition interface in the Suakin Deep, located at 2770 m in the central Red Sea, to reveal previously undocumented fine-scale community structuring and succession of metabolic groups along a salinity gradient only 1 m thick. Metagenomic profiling at a 10-cm-scale resolution highlighted spatial organization of key metabolic pathways and corresponding microbial functional units, emphasizing the prominent role and significance of salinity and oxygen in shaping their ecology. Nitrogen cycling processes are especially affected by the redoxcline with ammonia oxidation processes being taxa and layers specific, highlighting also the presence of novel microorganisms, such as novel Thaumarchaeota and anammox, adapted to the changing conditions of the chemocline. The findings render the transition zone as a critical niche for nitrogen cycling, with complementary metabolic networks, in turn underscoring the biogeochemical complexity of deep-sea brines.

Heterotrophic bacterioplankton responses in coral- and algae-dominated Red Sea reefs show they might benefit from future regime shift.

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.

Heterotrophic Bacterioplankton Growth and Physiological Properties in Red Sea Tropical Shallow Ecosystems With Different Dissolved Organic Matter Sources.

Despite the key role of heterotrophic bacterioplankton in the biogeochemistry of tropical coastal waters, their dynamics have been poorly investigated in relation to the different dissolved organic matter (DOM) pools usually available. In this study we conducted four seasonal incubations of unfiltered and predator-free seawater (Community and Filtered treatment, respectively) at three Red Sea coastal sites characterized by different dominant DOM sources: Seagrass, Mangrove, and Phytoplankton. Bacterial abundance, growth and physiological status were assessed by flow cytometry and community composition by 16S rRNA gene amplicons. The Seagrass site showed the highest initial abundances (6.93 ± 0.30 × 105 cells mL-1), coincident with maximum DOC concentrations (>100 µmol C L-1), while growth rates peaked at the Mangrove site (1.11 ± 0.09 d-1) and were consistently higher in the Filtered treatment. The ratio between the Filtered and Community maximum bacterial abundance (a proxy for top-down control by protistan grazers) showed minimum values at the Seagrass site (1.05 ± 0.05) and maximum at the Phytoplankton site (1.24 ± 0.30), suggesting protistan grazing was higher in open waters, especially in the first half of the year. Since the Mangrove and Seagrass sites shared a similar bacterial diversity, the unexpected lack of bacterial response to predators removal at the latter site should be explained by differences in DOM characteristics. Nitrogen-rich DOM and fluorescent protein-like components were significantly associated with enhanced specific growth rates along the inshore-offshore gradient. Our study confirms the hypotheses that top-down factors control bacterial standing stocks while specific growth rates are bottom-up controlled in representative Red Sea shallow, oligotrophic ecosystems.

High summer temperatures amplify functional differences between coral- and algae-dominated reef communities.

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 bimonthly 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), whereas carbon losses via respiration and dissolved organic carbon release 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 coral-algal phase shifts. Algae-dominated communities may outcompete coral-dominated communities because of 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.

Changes in Population Age-Structure Obscure the Temperature-Size Rule in Marine Cyanobacteria.

The temperature-size Rule (TSR) states that there is a negative relationship between ambient temperature and body size. This rule has been independently evaluated for different phases of the life cycle in multicellular eukaryotes, but mostly for the average population in unicellular organisms. We acclimated two model marine cyanobacterial strains (Prochlorococcus marinus MIT9301 and Synechococcus sp. RS9907) to a gradient of temperatures and measured the changes in population age-structure and cell size along their division cycle. Both strains displayed temperature-dependent diel changes in cell size, and as a result, the relationship between temperature and average cell size varied along the day. We computed the mean cell size of new-born cells in order to test the prediction of the TSR on a single-growth stage. Our work reconciles previous inconsistent results when testing the TSR on unicellular organisms, and shows that when a single-growth stage is considered the predicted negative response to temperature is revealed.