Investigating zinc toxicity responses in marine Prochlorococcus and Synechococcus.

Marine plastic pollution is a growing concern worldwide and has the potential to impact marine life via leaching of chemicals, with zinc (Zn), a common plastic additive, observed at particularly high levels in plastic leachates in previous studies. At this time, however, little is known regarding how elevated Zn affects key groups of marine primary producers. Marine cyanobacterial genera Prochlorococcus and Synechococcus are considered to be some of the most abundant oxygenic phototrophs on earth, and together contribute significantly to oceanic primary productivity. Here we set out to investigate how two Prochlorococcus (MIT9312 and NATL2A) and two Synechococcus (CC9311 and WH8102) strains, representative of diverse ecological niches, respond to exposure to high Zn concentrations. The two genera showed differences in the timing and degree of growth and physiological responses to elevated Zn levels, with Prochlorococcus strains showing declines in their growth rate and photophysiology following exposure to 27 µg l-1 Zn, while Synechococcus CC9311 and WH8102 growth rates declined significantly on exposure to 52 and 152 µg l-1 Zn, respectively. Differences were also observed in each strain's capacity to maintain cell wall integrity on exposure to different levels of Zn. Our results indicate that excess Zn has the potential to pose a challenge to some marine picocyanobacteria and highlights the need to better understand how different marine Prochlorococcus and Synechococcus strains may respond to increasing concentrations of Zn in some marine regions.

Co-culture with Synechococcus facilitates growth of Prochlorococcus under ocean acidification conditions.

Anthropogenic CO2 emissions are projected to lower the pH of the ocean 0.3 units by 2100. Previous studies suggested that Prochlorococcus and Synechococcus, the numerically dominant phytoplankton in the oceans, have different responses to elevated CO2 that may result in a dramatic shift in their relative abundances in future oceans. Here we showed that the exponential growth rates of these two genera respond to future CO2 conditions in a manner similar to other cyanobacteria, but Prochlorococcus strains had significantly lower realized growth rates under elevated CO2 regimes due to poor survival after exposure to fresh culture media. Despite this, a Synechococcus strain was unable to outcompete a Prochlorococcus strain in co-culture at elevated CO2 . Under these conditions, Prochlorococcus' poor response to elevated CO2 disappeared, and Prochlorococcus' relative fitness showed negative frequency dependence, with both competitors having significant fitness advantages when initially rare. These experiments suggested that the two strains should be able to coexist indefinitely in co-culture despite sharing nearly identical nutritional requirements. We speculate that negative frequency dependence exists due to reductive Black Queen evolution that has resulted in a passively mutualistic relationship analogous to that connecting Prochlorococcus with the 'helper' heterotrophic microbes in its environment.

Persistent El Niño driven shifts in marine cyanobacteria populations.

In the California Current Ecosystem, El Niño acts as a natural phenomenon that is partially representative of climate change impacts on marine bacteria at timescales relevant to microbial communities. Between 2014-2016, the North Pacific warm anomaly (a.k.a., the "blob") and an El Niño event resulted in prolonged ocean warming in the Southern California Bight (SCB). To determine whether this "marine heatwave" resulted in shifts in microbial populations, we sequenced the rpoC1 gene from the biogeochemically important picocyanobacteria Prochlorococcus and Synechococcus at 434 time points from 2009-2018 in the MICRO time series at Newport Beach, CA. Across the time series, we observed an increase in the abundance of Prochlorococcus relative to Synechococcus as well as elevated frequencies of ecotypes commonly associated with low-nutrient and high-temperature conditions. The relationships between environmental and ecotype trends appeared to operate on differing temporal scales. In contrast to ecotype trends, most microdiverse populations were static and possibly reflect local habitat conditions. The only exceptions were microdiversity from Prochlorococcous HLI and Synechococcus Clade II that shifted in response to the 2015 El Niño event. Overall, Prochlorococcus and Synechococcus populations did not return to their pre-heatwave composition by the end of this study. This research demonstrates that extended warming in the SCB can result in persistent changes in key microbial populations.

Prochlorococcus Cells Rely on Microbial Interactions Rather than on Chlorotic Resting Stages To Survive Long-Term Nutrient Starvation.

Many microorganisms produce resting cells with very low metabolic activity that allow them to survive phases of prolonged nutrient or energy stress. In cyanobacteria and some eukaryotic phytoplankton, the production of resting stages is accompanied by a loss of photosynthetic pigments, a process termed chlorosis. Here, we show that a chlorosis-like process occurs under multiple stress conditions in axenic laboratory cultures of Prochlorococcus, the dominant phytoplankton linage in large regions of the oligotrophic ocean and a global key player in ocean biogeochemical cycles. In Prochlorococcus strain MIT9313, chlorotic cells show reduced metabolic activity, measured as C and N uptake by Nanoscale secondary ion mass spectrometry (NanoSIMS). However, unlike many other cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not regrow under axenic conditions when transferred to new media. Nevertheless, cocultures with a heterotrophic bacterium, Alteromonas macleodii HOT1A3, allowed Prochlorococcus to survive nutrient starvation for months. We propose that reliance on co-occurring heterotrophic bacteria, rather than the ability to survive extended starvation as resting cells, underlies the ecological success of ProchlorococcusIMPORTANCE The ability of microorganisms to withstand long periods of nutrient starvation is key to their survival and success under highly fluctuating conditions that are common in nature. Therefore, one would expect this trait to be prevalent among organisms in the nutrient-poor open ocean. Here, we show that this is not the case for Prochlorococcus, a globally abundant and ecologically important marine cyanobacterium. Instead, Prochlorococcus relies on co-occurring heterotrophic bacteria to survive extended phases of nutrient and light starvation. Our results highlight the power of microbial interactions to drive major biogeochemical cycles in the ocean and elsewhere with consequences at the global scale.

Minimal cobalt metabolism in the marine cyanobacterium Prochlorococcus.

Despite very low concentrations of cobalt in marine waters, cyanobacteria in the genus Prochlorococcus retain the genetic machinery for the synthesis and use of cobalt-bearing cofactors (cobalamins) in their genomes. We explore cobalt metabolism in a Prochlorococcus isolate from the equatorial Pacific Ocean (strain MIT9215) through a series of growth experiments under iron- and cobalt-limiting conditions. Metal uptake rates, quantitative proteomic measurements of cobalamin-dependent enzymes, and theoretical calculations all indicate that Prochlorococcus MIT9215 can sustain growth with less than 50 cobalt atoms per cell, ∼100-fold lower than minimum iron requirements for these cells (∼5,100 atoms per cell). Quantitative descriptions of Prochlorococcus cobalt limitation are used to interpret the cobalt distribution in the equatorial Pacific Ocean, where surface concentrations are among the lowest measured globally but Prochlorococcus biomass is high. A low minimum cobalt quota ensures that other nutrients, notably iron, will be exhausted before cobalt can be fully depleted, helping to explain the persistence of cobalt-dependent metabolism in marine cyanobacteria.

Marine picoplankton size distribution and optical property contrasts throughout the Atlantic Ocean revealed using flow cytometry.

Depth-resolved flow cytometric observations have been used to determine the size distribution and refractive index (RI) of picoplankton throughout the Atlantic Ocean. Prochlorococcus frequently showed double size distribution peaks centered on ${0.75 \pm 0.25}$0.75±0.25 and ${1.75 \pm 0.25}\,\,{\rm \unicode{x00B5}{\rm m}}$1.75±0.25µm; the smallest peak diameters were ${\le}{0.65}\,\,{\rm \unicode{x00B5}{\rm m}}$≤0.65µm in the equatorial upwelling with larger cells (${\sim}{0.95}\,\,{\rm \unicode{x00B5}{\rm m}}$∼0.95µm) in the surface layers of the tropical gyres. Synechococcus was strongly monodispersed: the smallest (${\sim}{1.5}\,\,{\rm \unicode{x00B5}{\rm m}}$∼1.5µm) and largest cells (${\sim}{2.25{-}2.50}\,\,{\rm \unicode{x00B5}{\rm m}}$∼2.25-2.50µm) were encountered in the lowest and highest abundance regions, respectively. Typical RI for Prochlorococcus was found to be ${\sim}{1.06}$∼1.06, whereas for Synechococcus surface RI varied between 1.04-1.08 at high and low abundances, respectively.

Resistance in marine cyanobacteria differs against specialist and generalist cyanophages.

Long-term coexistence between unicellular cyanobacteria and their lytic viruses (cyanophages) in the oceans is thought to be due to the presence of sensitive cells in which cyanophages reproduce, ultimately killing the cell, while other cyanobacteria survive due to resistance to infection. Here, we investigated resistance in marine cyanobacteria from the genera Synechococcus and Prochlorococcus and compared modes of resistance against specialist and generalist cyanophages belonging to the T7-like and T4-like cyanophage families. Resistance was extracellular in most interactions against specialist cyanophages irrespective of the phage family, preventing entry into the cell. In contrast, resistance was intracellular in practically all interactions against generalist T4-like cyanophages. The stage of intracellular arrest was interaction-specific, halting at various stages of the infection cycle. Incomplete infection cycles proceeded to various degrees of phage genome transcription and translation as well as phage genome replication in numerous interactions. In a particularly intriguing case, intracellular capsid assembly was observed, but the phage genome was not packaged. The cyanobacteria survived the encounter despite late-stage infection and partial genome degradation. We hypothesize that this is tolerated due to genome polyploidy, which we found for certain strains of both Synechococcus and Prochlorococcus Our findings unveil a heavy cost of promiscuous entry of generalist phages into nonhost cells that is rarely paid by specialist phages and suggests the presence of unknown mechanisms of intracellular resistance in the marine unicellular cyanobacteria. Furthermore, these findings indicate that the range for virus-mediated horizontal gene transfer extends beyond hosts to nonhost cyanobacterial cells.

Plastic leachates impair growth and oxygen production in Prochlorococcus, the ocean's most abundant photosynthetic bacteria.

Plastic pollution is a global threat to marine ecosystems. Plastic litter can leach a variety of substances into marine environments; however, virtually nothing is known regarding how this affects photosynthetic bacteria at the base of the marine food web. To address this, we investigated the effect of plastic leachate exposure on marine Prochlorococcus, widely considered the most abundant photosynthetic organism on Earth and vital contributors to global primary production and carbon cycling. Two strains of Prochlorococcus representing distinct ecotypes were exposed to leachate from common plastic items: high-density polyethylene bags and polyvinyl chloride matting. We show leachate exposure strongly impairs Prochlorococcus in vitro growth and photosynthetic capacity and results in genome-wide transcriptional changes. The strains showed distinct differences in the extent and timing of their response to each leachate. Consequently, plastic leachate exposure could influence marine Prochlorococcus community composition and potentially the broader composition and productivity of ocean phytoplankton communities.

A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton.

In many regions of the world oceans, phytoplankton face the problem of discriminating between phosphate, an essential nutrient, and arsenate, a toxic analogue. Many phytoplankton, including the most abundant phytoplankton group known, Prochlorococcus, detoxify arsenate (AsV) by reduction to arsenite (AsIII), followed by methylation and excretion of the methylated arsenic products. We synthesized [14C]dimethyl arsenate (DMA) and used it to show that cultured Pelagibacter strain HTCC7211 (SAR11) cells oxidize the methyl group carbons of DMA, producing 14CO2 and ATP. We measured [14C]DMA oxidation rates in the P-depleted surface waters of the Sargasso Sea, a subtropical ocean gyre. [14C]DMA was oxidized to 14CO2 by Sargasso Sea plankton communities at a rate that would cause turnover of the estimated DMA standing stock every 8.1 days. SAR11 strain HTCC7211, which was isolated from the Sargasso Sea, has a pair of arsenate resistance genes and was resistant to arsenate, showing no growth inhibition at As/P ratios of >65:1. Across the global oceans, there was a strong inverse relationship between the frequency of the arsenate reductase (LMWPc_ArsC) in Pelagibacter genomes and phosphate concentrations. We propose that the demethylation of methylated arsenic compounds by Pelagibacter and possibly other bacterioplankton, coupled with arsenate resistance, results in the transfer of energy from phytoplankton to bacteria. We dub this a parasitic cycle because the release of arsenate by Pelagibacter in principle creates a positive-feedback loop that forces phytoplankton to continually regenerate arsenate detoxification products, producing a flow of energy to P-limited ocean regions.IMPORTANCE In vast, warm regions of the oceans, phytoplankton face the problem of arsenic poisoning. Arsenate is toxic because it is chemically similar to phosphate, a scarce nutrient that phytoplankton cells need for growth. Many phytoplankton, including the commonest phytoplankton type in warm oceans, Prochlorococcus, detoxify arsenate by adding methyl groups. Here we show that the most abundant non-photosynthetic plankton in the oceans, SAR11 bacteria, remove the methyl groups, releasing poisonous forms of arsenic back into the water. We postulate that the methylation and demethylation of arsenic compounds creates a cycle in which the phytoplankton can never get ahead and must continually transfer energy to the SAR11 bacteria. We dub this a parasitic process and suggest that it might help explain why SAR11 bacteria are so successful, surpassing all other plankton in their numbers. Field experiments were done in the Sargasso Sea, a subtropical ocean gyre that is sometimes called an ocean desert because, throughout much of the year, there is not enough phosphorous in the water to support large blooms of phytoplankton. Ocean deserts are expanding as the oceans absorb heat and grow warmer.

Co-culture and biogeography of Prochlorococcus and SAR11.

Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15-70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11's central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 - highlighting the biogeochemical potential of these two groups.

Picophytoplankton size and biomass around equatorial eastern Indian Ocean.

The cellular size and biomass of picophytoplankton were studied by flow cytometer during spring monsoon (March-May of 2015) in equatorial eastern Indian Ocean. We established an empirical relationship between forward scatter and cellular size to address the size and biomass of picophytoplankton. Results indicated that mean cell diameter of Prochlorococcus (0.60 µm) was the smallest, and then followed by Synechococcus (0.98 µm) and picoeukaryotic phytoplankton (1.05 µm). Thereafter, the biomass converted by abundance reached 0.64 µg·C·L-1 for Prochlorococcus, 0.34 µg·C·L-1 for Synechococcus, and 0.20 µg·C·L-1 for picoeukaryotic phytoplankton. Additionally, the distinct biomass contribution of picophytoplankton appeared to be affected by abundance, but not changes in cellular size. Vertically, the cellular sizes of picophytoplankton were remarkably small in upper waters, which was predominantly controlled by the nutrient availability. In contrast, they were larger in deeper waters, which was primarily attributed to the combined effects of low temperature and reduced light availability. Spatially, under the influence of high nutrient concentration induced by the different circulations and coastal upwelling, slightly high carbon biomass of picophytoplankton was observed around the coastal zones of Sri Lanka island and Sumatra, as well as the southern Bay of Bengal.

NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton.

Nitrogen (N) is a limiting nutrient in vast regions of the world's oceans, yet the sources of N available to various phytoplankton groups remain poorly understood. In this study, we investigated inorganic carbon (C) fixation rates and nitrate (NO3-), ammonium (NH4+) and urea uptake rates at the single cell level in photosynthetic pico-eukaryotes (PPE) and the cyanobacteria Prochlorococcus and Synechococcus. To that end, we used dual 15N and 13C-labeled incubation assays coupled to flow cytometry cell sorting and nanoSIMS analysis on samples collected in the North Pacific Subtropical Gyre (NPSG) and in the California Current System (CCS). Based on these analyses, we found that photosynthetic growth rates (based on C fixation) of PPE were higher in the CCS than in the NSPG, while the opposite was observed for Prochlorococcus. Reduced forms of N (NH4+ and urea) accounted for the majority of N acquisition for all the groups studied. NO3- represented a reduced fraction of total N uptake in all groups but was higher in PPE (17.4 ± 11.2% on average) than in Prochlorococcus and Synechococcus (4.5 ± 6.5 and 2.9 ± 2.1% on average, respectively). This may in part explain the contrasting biogeography of these picoplankton groups. Moreover, single cell analyses reveal that cell-to-cell heterogeneity within picoplankton groups was significantly greater for NO3- uptake than for C fixation and NH4+ uptake. We hypothesize that cellular heterogeneity in NO3- uptake within groups facilitates adaptation to the fluctuating availability of NO3- in the environment.

Ediacara biota flourished in oligotrophic and bacterially dominated marine environments across Baltica.

Middle-to-late Ediacaran (575-541 Ma) marine sedimentary rocks record the first appearance of macroscopic, multicellular body fossils, yet little is known about the environments and food sources that sustained this enigmatic fauna. Here, we perform a lipid biomarker and stable isotope (δ15Ntotal and δ13CTOC) investigation of exceptionally immature late Ediacaran strata (<560 Ma) from multiple locations across Baltica. Our results show that the biomarker assemblages encompass an exceptionally wide range of hopane/sterane ratios (1.6-119), which is a broad measure of bacterial/eukaryotic source organism inputs. These include some unusually high hopane/sterane ratios (22-119), particularly during the peak in diversity and abundance of the Ediacara biota. A high contribution of bacteria to the overall low productivity may have bolstered a microbial loop, locally sustaining dissolved organic matter as an important organic nutrient. These oligotrophic, shallow-marine conditions extended over hundreds of kilometers across Baltica and persisted for more than 10 million years.

Cross-protection from hydrogen peroxide by helper microbes: the impacts on the cyanobacterium Prochlorococcus and other beneficiaries in marine communities.

Hydrogen peroxide (HOOH) is a reactive oxygen species, derived from molecular oxygen, that is capable of damaging microbial cells. Surprisingly, the HOOH defence systems of some aerobes in the oxygenated marine environments are critically depleted, relative to model aerobes. For instance, the gene encoding catalase is absent in the numerically dominant photosynthetic cyanobacterium, Prochlorococcus. Accordingly, Prochlorococcus is highly susceptible to HOOH when exposed as pure cultures. Pure cultures do not exist in the marine environment, however. Catalase-positive community members can remove HOOH from the seawater medium, thus lowering the threat to Prochlorococcus and any other member that likewise lacks their own catalase. This cross-protection may constitute a loosely defined symbiosis, whereby the catalase-positive helper cells may benefit through the acquisition of nutrients released by the beneficiaries such as Prochlorococcus. Other members of the community that may be helped by the catalase-positive cells may include some lineages of Synechococcus - the sister genus of Prochlorococcus - as well as some lineages of SAR11 and ammonia oxidizing archaea and bacteria. The co-occurrence of catalase-positive and -negative members suggests that cross-protection from HOOH-mediated oxidative stress may play an important role in the construction of the marine microbial community.

Distinct features of C/N balance regulation in Prochlorococcus sp. strain MIT9313.

The abundance and significant contribution to global primary production of the marine cyanobacterium Prochlorococcus have made it one of the main models in marine ecology. Several conditions known to cause strong effects on the regulation of N-related enzymes in other cyanobacteria lacked such effect in Prochlorococcus. Prochlorococcus sp. strain MIT9313 is one of the most early-branching strains among the members of this genus. In order to further understand the C/N control system in this cyanobacterium, we studied the effect of the absence of three key elements in the ocean, namely N, P and Fe, as well as the effect of inhibitors of the N assimilation or photosynthesis on the N metabolism of this strain. Furthermore, we focused our work in the effect of ageing, as the age of cultures has clear effects on the regulation of some enzymes in Prochlorococcus. To reach this goal, expression of the main three regulators involved in N assimilation in cyanobacteria, namely ntcA, glnB and pipX, as well as that of icd (encoding for isocitrate dehydrogenase) were analysed. Our results show that the control of the main proteins involved in the C/N balance in strain MIT9313 differs from other model Prochlorococcus strains.

Seasonal variability of picophytoplankton under contrasting environments in northern Tunisian coasts, southwestern Mediterranean Sea.

We investigated at the single cell level during 16months (June 2012 to September 2013) the temporal distribution of picophytoplankton (picoeukaryotes, Synechococcus and Prochlorococcus) communities in two contrasted ecosystems: the Bay of Bizerte characterised by an oligotrophic regime typical of the Mediterranean Sea and the Bizerte Lagoon that exhibits a mesotrophic/eutrophic state. We aimed at depicting seasonal variations and quantifying the relationships between the environmental factors and the structure and abundance of picophytoplankton communities. Results showed that picophytoplankton groups were able to grow under a wide range of environmental conditions varying seasonally, although their abundances and contributions to the total chlorophyll biomass significantly varied and showed importance in the Bay of Bizerte. Synechococcus was the most abundant group reaching 225∗103cells·cm-3 in the Bay and 278∗103cells·cm-3 in the lagoon. This group was present all over the year in both ecosystems. Structural equation model results pointed out a different configuration regarding the picophytoplankton environmental drivers. The complexity of the configuration, i.e. number of significant links within the system, decreased under enhanced eutrophication conditions. The less exposure to anthropogenic stress, i.e. in the Bay of Bizerte, highlight a larger role of nutrient and hydrological conditions on the seasonal variations of picophytoplankton, whereas a negative effect of eutrophication on picophytoplankton communities was unveiled in the Bizerte Lagoon. We stress that such influence may be exacerbated under expected scenarios of Mediterranean warming conditions and nutrient release in coastal ecosystems.

Photoinhibition in marine picocyanobacteria.

Marine Synechococcus and Prochlorococcus cyanobacteria have different antenna compositions although they are genetically near to each other, and different strains thrive in very different illumination conditions. We measured growth and photoinhibition of PSII in two low-light and one high-light Prochlorococcus strains and in one Synechococcus strain. All strains were found to be able to shortly utilize moderate or even high light, but the low-light strains bleached rapidly in moderate light. Measurements of photoinhibition in the presence of the antibiotic lincomycin showed that a low-light Prochlorococcus strain was more sensitive than a high-light strain and both were more sensitive than the marine Synechococcus. The action spectrum of photoinhibition showed an increase from blue to ultraviolet wavelengths in all strains, suggesting contribution of manganese absorption to photoinhibition, but blue light caused less photoinhibition in marine cyanobacteria than expected on the basis of earlier results from plants and cyanobacteria. The visible-light part of the action spectrum resembled the absorption spectrum of the organism, suggesting that photosynthetic antenna pigments, especially divinyl chlorophylls, have a more important role as photoreceptors of visible-light photoinhibition in marine cyanobacteria than in other photoautotrophs.

Metabolic evolution and the self-organization of ecosystems.

Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus To understand what drove observed evolutionary patterns, we interpreted them in the context of its population dynamics, growth rate, and light adaptation, and the size and macromolecular and elemental composition of cells. This multilevel view suggests that, over the course of evolution, there was a steady increase in Prochlorococcus' metabolic rate and excretion of organic carbon. We derived a mathematical framework that suggests these adaptations lower the minimal subsistence nutrient concentration of cells, which results in a drawdown of nutrients in oceanic surface waters. This, in turn, increases total ecosystem biomass and promotes the coevolution of all cells in the ecosystem. Additional reconstructions suggest that Prochlorococcus and the dominant cooccurring heterotrophic bacterium SAR11 form a coevolved mutualism that maximizes their collective metabolic rate by recycling organic carbon through complementary excretion and uptake pathways. Moreover, the metabolic codependencies of Prochlorococcus and SAR11 are highly similar to those of chloroplasts and mitochondria within plant cells. These observations lead us to propose a general theory relating metabolic evolution to the self-amplification and self-organization of the biosphere. We discuss the implications of this framework for the evolution of Earth's biogeochemical cycles and the rise of atmospheric oxygen.

Interactions between Thermal Acclimation, Growth Rate, and Phylogeny Influence Prochlorococcus Elemental Stoichiometry.

Variability in plankton elemental requirements can be important for global ocean biogeochemistry but we currently have a limited understanding of how ocean temperature influences the plankton C/N/P ratio. Multiple studies have put forward a 'translation-compensation' hypothesis to describe the positive relationship between temperature and plankton N/P or C/P as cells should have lower demand for P-rich ribosomes and associated depressed QP when growing at higher temperature. However, temperature affects many cellular processes beyond translation with unknown outcomes on cellular elemental composition. In addition, the impact of temperature on growth and elemental composition of phytoplankton is likely modulated by the life history and growth rate of the organism. To test the direct and indirect (via growth rate changes) effect of temperature, we here analyzed the elemental composition and ratios in six strains affiliated with the globally abundant marine Cyanobacteria Prochlorococcus. We found that temperature had a significant positive effect on the carbon and nitrogen cell quota, whereas no clear trend was observed for the phosphorus cell quota. The effect on N/P and C/P were marginally significantly positive across Prochlorococcus. The elemental composition and ratios of individual strains were also affected but we found complex interactions between the strain identity, temperature, and growth rate in controlling the individual elemental ratios in Prochlorococcus and no common trends emerged. Thus, the observations presented here does not support the 'translation-compensation' theory and instead suggest unique cellular elemental effects as a result of rising temperature among closely related phytoplankton lineages. Thus, the biodiversity context should be considered when predicting future elemental ratios and how cycles of carbon, nitrogen, and phosphorus may change in a future ocean.

Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean.

Viral lysis of phytoplankton constrains marine primary production, food web dynamics and biogeochemical cycles in the ocean. Yet, little is known about the biogeographical distribution of viral lysis rates across the global ocean. To address this, we investigated phytoplankton group-specific viral lysis rates along a latitudinal gradient within the North Atlantic Ocean. The data show large-scale distribution patterns of different virus groups across the North Atlantic that are associated with the biogeographical distributions of their potential microbial hosts. Average virus-mediated lysis rates of the picocyanobacteria Prochlorococcus and Synechococcus were lower than those of the picoeukaryotic and nanoeukaryotic phytoplankton (that is, 0.14 per day compared with 0.19 and 0.23 per day, respectively). Total phytoplankton mortality (virus plus grazer-mediated) was comparable to the gross growth rate, demonstrating high turnover rates of phytoplankton populations. Virus-induced mortality was an important loss process at low and mid latitudes, whereas phytoplankton mortality was dominated by microzooplankton grazing at higher latitudes (>56°N). This shift from a viral-lysis-dominated to a grazing-dominated phytoplankton community was associated with a decrease in temperature and salinity, and the decrease in viral lysis rates was also associated with increased vertical mixing at higher latitudes. Ocean-climate models predict that surface warming will lead to an expansion of the stratified and oligotrophic regions of the world's oceans. Our findings suggest that these future shifts in the regional climate of the ocean surface layer are likely to increase the contribution of viral lysis to phytoplankton mortality in the higher-latitude waters of the North Atlantic, which may potentially reduce transfer of matter and energy up the food chain and thus affect the capacity of the northern North Atlantic to act as a long-term sink for CO2.