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Nutrient availability limits phytoplankton growth throughout much of the global ocean. Here we synthesize available experimental data to identify three dominant nutrient limitation regimes: nitrogen is limiting in the stratified subtropical gyres and in the summertime Arctic Ocean, iron is most commonly limiting in upwelling regions, and both nutrients are frequently co-limiting in regions in between the nitrogen and iron limited systems. Manganese can be co-limiting with iron in parts of the Southern Ocean, whilst phosphate and cobalt can be co-/serially limiting in some settings. Overall, an analysis of experimental responses showed that phytoplankton net growth can be significantly enhanced through increasing the number of different nutrients supplied, regardless of latitude, temperature, or trophic status, implying surface seawaters are often approaching nutrient co-limitation. Assessments of nutrient deficiency based on seawater nutrient concentrations and nutrient stress diagnosed via molecular biomarkers showed good agreement with experimentally-assessed nutrient limitation, validating conceptual and theoretical links between nutrient stoichiometry and microbial ecophysiology. Nutrient limitation is a key constraint on ocean productivity. Here, by analysing a compilation of field experiments spanning the global ocean, this study shows that increasing the number of different nutrients supplied significantly increases net phytoplankton growth, suggesting multiple nutrients are often approaching co-limiting levels.

Ecosystems are controlled by ‘bottom-up’ (resources) and ‘top-down’ (predation) forces. Viral infection is now recognized as a ubiquitous top-down control of microbial growth across ecosystems but, at the same time, cell death by viral predation influences, and is influenced by, resource availability. In this Review, we discuss recent advances in understanding the biogeochemical impact of viruses, focusing on how metabolic reprogramming of host cells during lytic viral infection alters the flow of energy and nutrients in aquatic ecosystems. Our synthesis revealed several emerging themes. First, viral infection transforms host metabolism, in part through virus-encoded metabolic genes; the functions performed by these genes appear to alleviate energetic and biosynthetic bottlenecks to viral production. Second, viral infection depends on the physiological state of the host cell and on environmental conditions, which are challenging to replicate in the laboratory. Last, metabolic reprogramming of infected cells and viral lysis alter nutrient cycling and carbon export in the oceans, although the net impacts remain uncertain. This Review highlights the need for understanding viral infection dynamics in realistic physiological and environmental contexts to better predict their biogeochemical consequences.

Marine phytoplankton generate half of global primary production, making them essential to ecosystem functioning and biogeochemical cycling. Though phytoplankton are phylogenetically diverse, studies rarely designate unique thermal traits to different taxa, resulting in coarse representations of phytoplankton thermal responses. Here we assessed phytoplankton functional responses to temperature using empirically derived thermal growth rates from four principal contributors to marine productivity: diatoms, dinoflagellates, cyanobacteria, and coccolithophores. Using modeled sea surface temperatures for 1950–1970 and 2080–2100, we explored potential alterations to each group’s growth rates and geographical distribution under a future climate change scenario. Contrary to the commonly applied Eppley formulation, our data suggest phytoplankton functional types may be characterized by different temperature coefficients (Q 10 ), growth maxima thermal dependencies, and thermal ranges which would drive dissimilar responses to each degree of temperature change. These differences, when applied in response to global simulations of future temperature, result in taxon-specific projections of growth and geographic distribution, with low-latitude coccolithophores facing considerable decreases and cyanobacteria substantial increases in growth rates. These results suggest that the singular effect of changing temperature may alter phytoplankton global community structure, owing to the significant variability in thermal response between phytoplankton functional types. Phytoplankton communities are important players in biogeochemical processes, but are sensitive to global warming. Here, a meta-analysis shows how the varied responses of phytoplankton to rising temperatures could potentially alter growth dynamics and community structure in a future ocean.

The assembly and analysis of complete genomes and large genomic fragments have tripled the number of known ocean viruses and uncovered the potentially important roles they play in nitrogen and sulfur cycling. Viral diversity in the oceans Ocean viruses profoundly impact microbial community composition and metabolic activity in the oceans, thereby affecting global-scale biogeochemical cycling. Owing to sampling and cultivation challenges, viral diversity remains poorly described at the genome level, such that less than one per cent of observed surface-ocean viruses are 'known'. Information on viruses of the deep ocean is particularly scarce. Here, Matthew Sullivan and colleagues report the assembly of complete genomes and large genomic fragments from both surface- and deep-ocean viruses sampled during the Tara Oceans and Malaspina research expeditions. The resulting Global Oceans Viromes dataset roughly triples known ocean viral populations and doubles known candidate bacterial and archaeal viral genera. Using this global map, the study predicts viral hosts and identifies viral auxiliary metabolic genes, most of which were previously unknown. Ocean microbes drive biogeochemical cycling on a global scale 1 . However, this cycling is constrained by viruses that affect community composition, metabolic activity, and evolutionary trajectories 2 , 3 . Owing to challenges with the sampling and cultivation of viruses, genome-level viral diversity remains poorly described and grossly understudied, with less than 1% of observed surface-ocean viruses known 4 . Here we assemble complete genomes and large genomic fragments from both surface- and deep-ocean viruses sampled during the Tara Oceans and Malaspina research expeditions 5 , 6 , and analyse the resulting ‘global ocean virome’ dataset to present a global map of abundant, double-stranded DNA viruses complete with genomic and ecological contexts. A total of 15,222 epipelagic and mesopelagic viral populations were identified, comprising 867 viral clusters (defined as approximately genus-level groups 7 , 8 ). This roughly triples the number of known ocean viral populations 4 and doubles the number of candidate bacterial and archaeal virus genera 8 , providing a near-complete sampling of epipelagic communities at both the population and viral-cluster level. We found that 38 of the 867 viral clusters were locally or globally abundant, together accounting for nearly half of the viral populations in any global ocean virome sample. While two-thirds of these clusters represent newly described viruses lacking any cultivated representative, most could be computationally linked to dominant, ecologically relevant microbial hosts. Moreover, we identified 243 viral-encoded auxiliary metabolic genes, of which only 95 were previously known. Deeper analyses of four of these auxiliary metabolic genes ( dsrC , soxYZ , P-II (also known as glnB ) and amoC ) revealed that abundant viruses may directly manipulate sulfur and nitrogen cycling throughout the epipelagic ocean. This viral catalog and functional analyses provide a necessary foundation for the meaningful integration of viruses into ecosystem models where they act as key players in nutrient cycling and trophic networks.

An analysis of 24 coral reef viromes challenges the view that lytic phage are believed to predominate when the density of their hosts increase and shows instead that lysogeny is more important at high host densities; the authors also show that this model is consistent with predator–prey dynamics in a range of other ecosystems, such as animal-associated, sediment and soil systems. Microbial viruses can control host abundances via density-dependent lytic predator–prey dynamics. Less clear is how temperate viruses, which coexist and replicate with their host, influence microbial communities. Here we show that virus-like particles are relatively less abundant at high host densities. This suggests suppressed lysis where established models predict lytic dynamics are favoured. Meta-analysis of published viral and microbial densities showed that this trend was widespread in diverse ecosystems ranging from soil to freshwater to human lungs. Experimental manipulations showed viral densities more consistent with temperate than lytic life cycles at increasing microbial abundance. An analysis of 24 coral reef viromes showed a relative increase in the abundance of hallmark genes encoded by temperate viruses with increased microbial abundance. Based on these four lines of evidence, we propose the Piggyback-the-Winner model wherein temperate dynamics become increasingly important in ecosystems with high microbial densities; thus ‘more microbes, fewer viruses’. Live-and-let-live marine phage Lytic phage can control the abundance of their microbial hosts in a density-dependent manner with 'kill-the-winner' predation dynamics. It was widely assumed that lytic phages would dominate in nutrient-rich conditions favouring high host density, and that lysogenic phage, which integrate into their hosts instead of lysing them, tend to dominate when host numbers are low. This meta-analysis of 24 coral reef viromes challenges that view. Ben Knowles et al . find that lysogeny is more important than lysis at high, rather than low host densities. The authors term this the 'Piggyback-the-Winner' model, and show that it is consistent with predator–prey dynamics in a range of other ecosystems, including animal-associated, sediment, and soil systems.

A third or more of the fixed nitrogen lost from the oceans as N 2 is removed by anaerobic microbial processes in open ocean oxygen minimum zones. These zones have expanded over the past decades, and further anthropogenically induced expansion could accelerate nitrogen loss. However, in the Bay of Bengal there has been no indication of nitrogen loss, although oxygen levels are below the detection level of conventional methods (1 to 2 μM). Here we quantify the abundance of microbial genes associated with N 2 production, measure nitrogen transformations in incubations of sampled seawater with isotopically labelled nitrogen compounds and analyse geochemical signatures of these processes in the water column. We find that the Bay of Bengal supports denitrifier and anammox microbial populations, mediating low, but significant N loss. Yet, unlike other oxygen minimum zones, our measurements using a highly sensitive oxygen sensor demonstrate that the Bay of Bengal has persistent concentrations of oxygen in the 10 to 200 nM range. We propose that this oxygen supports nitrite oxidation, thereby restricting the nitrite available for anammox or denitrification. If these traces of oxygen were removed, nitrogen loss in the Bay of Bengal oxygen minimum zone waters could accelerate to global significance. Nitrogen losses have not been observed in the Bay of Bengal, unlike in other ocean oxygen minimum zones. Chemical and molecular analyses reveal that trace levels of oxygen inhibit nitrate formation, largely preventing microbial N 2 production.

The discovery of chemosynthetic ecosystems at deep-sea hydrothermal vents in 1977 changed our view of biology. Chemosynthetic bacteria and archaea form the foundation of vent ecosystems by exploiting the chemical disequilibrium between reducing hydrothermal fluids and oxidizing seawater, harnessing this energy to fix inorganic carbon into biomass. Recent research has uncovered fundamental aspects of these microbial communities, including their relationships with underlying geology and hydrothermal geochemistry, interactions with animals via symbiosis and distribution both locally in various habitats within vent fields and globally across hydrothermal systems in diverse settings. Although ‘black smokers’ and symbioses between microorganisms and macrofauna attract much attention owing to their novelty and the insights they provide into life under extreme conditions, habitats such as regions of diffuse flow, subseafloor aquifers and hydrothermal plumes have important roles in the global cycling of elements through hydrothermal systems. Owing to sharp contrasts in physical and chemical conditions between these various habitats and their dynamic, extreme and geographically isolated nature, hydrothermal vents provide a valuable window into the environmental and ecological forces that shape microbial communities and insights into the limits, origins and evolution of microbial life.Hydrothermal vents are unique habitats for chemosynthetic bacteria and archaea and the animals that live in symbiosis with them. In this Review, Dick explores the challenges and opportunities that vent ecosystems provide for microbial life and their relationship to biogeography.

Sinking particulate organic carbon out of the surface ocean sequesters carbon on decadal to millennial timescales. Predicting the particulate carbon flux is therefore critical for understanding both global carbon cycling and the future climate. Microbes play a crucial role in particulate organic carbon degradation, but the impact of depth-dependent microbial dynamics on ocean-scale particulate carbon fluxes is poorly understood. Here we scale-up essential features of particle-associated microbial dynamics to understand the large-scale vertical carbon flux in the ocean. Our model provides mechanistic insight into the microbial contribution to the particulate organic carbon flux profile. We show that the enhanced transfer of carbon to depth can result from populations struggling to establish colonies on sinking particles due to diffusive nutrient loss, cell detachment, and mortality. These dynamics are controlled by the interaction between multiple biotic and abiotic factors. Accurately capturing particle-microbe interactions is essential for predicting variability in large-scale carbon cycling. Micro-scale microbial community dynamics can substantially alter the fate of sinking particulates in the ocean thus playing a key role in setting the vertical flux of particulate carbon in the ocean.

The leakage of cold, methane-rich fluids from subsurface reservoirs to the sea floor sustains some of the richest ecosystems on the sea bed. These cold-seep communities consume around two orders of magnitude more oxygen than the surrounding sea floor as a result of the microbial consumption of seep methane. The leakage of cold, methane-rich fluids from subsurface reservoirs to the sea floor at specific sites on continental slopes, termed cold seeps, sustains some of the richest ecosystems on the sea bed. These seep-fuelled communities utilize around two orders of magnitude more oxygen per unit area than non-seep seafloor communities. Much of the oxygen is consumed by microbes and animal–microbe symbioses that use methane as an energy source. The proportion of methane consumed varies with fluid flow rate, ranging from 80% in seeps with slow fluid flow to less than 20% in seeps where fluid flow is high. Assuming the presence of a few tens of thousands of active cold seep systems on continental slopes worldwide, we estimate that the total efflux of methane to the overlying ocean could reach 0.02 Gt of carbon annually. As much more methane is lost from continental slopes, be it through emission to the hydrosphere or consumption by microbes, than can be produced, we suggest that a substantial fraction of the methane that fuels seep ecosystems is sourced from deep carbon buried kilometres under the sea floor.

Molecular characterization of interactions between a globally distributed marine diatom and its bacterial consortium. Interactions between phytoplankton and marine bacteria Experimental difficulties mean that little is known about the interplay between phytoplankton and bacteria that provides the foundation of marine ecosystems. Here Virginia Armbrust and colleagues use a laboratory model system to characterize a bacterial consortium associated with a globally distributed diatom. They find that in consortium culture experiments Sulfitobacter sp. promote cell division in the diatom Pseudo-nitzschia multiseries through secretion of the indole-3-acetic acid (IAA), which is synthesized from both diatom-secreted and endogenous tryptophan. The authors use metabolomics and metatranscriptomics to identify IAA and some of the genes associated with IAA production in the ocean, although further work will be needed to fully investigate the ecological relevance of the pathway identified in the laboratory. This study is among the first to characterize at the molecular level the currency used to support a microbial consortium in the ocean and lays the groundwork for future efforts. Interactions between primary producers and bacteria impact the physiology of both partners, alter the chemistry of their environment, and shape ecosystem diversity 1 , 2 . In marine ecosystems, these interactions are difficult to study partly because the major photosynthetic organisms are microscopic, unicellular phytoplankton 3 . Coastal phytoplankton communities are dominated by diatoms, which generate approximately 40% of marine primary production and form the base of many marine food webs 4 . Diatoms co-occur with specific bacterial taxa 3 , but the mechanisms of potential interactions are mostly unknown. Here we tease apart a bacterial consortium associated with a globally distributed diatom and find that a Sulfitobacter species promotes diatom cell division via secretion of the hormone indole-3-acetic acid, synthesized by the bacterium using both diatom-secreted and endogenous tryptophan. Indole-3-acetic acid and tryptophan serve as signalling molecules that are part of a complex exchange of nutrients, including diatom-excreted organosulfur molecules and bacterial-excreted ammonia. The potential prevalence of this mode of signalling in the oceans is corroborated by metabolite and metatranscriptome analyses that show widespread indole-3-acetic acid production by Sulfitobacter- related bacteria, particularly in coastal environments. Our study expands on the emerging recognition that marine microbial communities are part of tightly connected networks by providing evidence that these interactions are mediated through production and exchange of infochemicals.