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A lot of methane is emitted from oxygenated seawater, where its production should be inhibited. Seawater incubations and organic matter characterizations reveal that bacteria aerobically produce methane from phosphonates in organic matter. Biogenic methane is widely thought to be a product of archaeal methanogenesis, an anaerobic process that is inhibited or outcompeted by the presence of oxygen and sulfate 1 , 2 , 3 . Yet a large fraction of marine methane delivered to the atmosphere is produced in high-sulfate, fully oxygenated surface waters that have methane concentrations above atmospheric equilibrium values, an unexplained phenomenon referred to as the marine methane paradox 4 , 5 . Here we use nuclear magnetic resonance spectroscopy to show that polysaccharide esters of three phosphonic acids are important constituents of dissolved organic matter in seawater from the North Pacific. In seawater and pure culture incubations, bacterial degradation of these dissolved organic matter phosphonates in the presence of oxygen releases methane, ethylene and propylene gas. Moreover, we found that in mutants of a methane-producing marine bacterium, Pseudomonas stutzeri , disrupted in the C–P lyase phosphonate degradation pathway, methanogenesis was also disabled, indicating that the C–P lyase pathway can catalyse methane production from marine dissolved organic matter. Finally, the carbon stable isotope ratio of methane emitted during our incubations agrees well with anomalous isotopic characteristics of seawater methane. We estimate that daily cycling of only about 0.25% of the organic matter phosphonate inventory would support the entire atmospheric methane flux at our study site. We conclude that aerobic bacterial degradation of phosphonate esters in dissolved organic matter may explain the marine methane paradox.

Nearly all iron dissolved in the ocean is complexed by strong organic ligands of unknown composition. The effect of ligand composition on microbial iron acquisition is poorly understood, but amendment experiments using model ligands show they can facilitate or impede iron uptake depending on their identity. Here we show that siderophores, organic compounds synthesized by microbes to facilitate iron uptake, are a dynamic component of the marine ligand pool in the eastern tropical Pacific Ocean. Siderophore concentrations in iron-deficient waters averaged 9 pM, up to fivefold higher than in iron-rich coastal and nutrient-depleted oligotrophic waters, and were dominated by amphibactins, amphiphilic siderophores with cell membrane affinity. Phylogenetic analysis of amphibactin biosynthetic genes suggests that the ability to produce amphibactins has transferred horizontally across multiple Gammaproteobacteria, potentially driven by pressures to compete for iron. In coastal and oligotrophic regions of the eastern Pacific Ocean, amphibactins were replaced with lower concentrations (1–2 pM) of hydrophilic ferrioxamine siderophores. Our results suggest that organic ligand composition changes across the surface ocean in response to environmental pressures. Hydrophilic siderophores are predominantly found across regions of the ocean where iron is not expected to be the limiting nutrient for the microbial community at large. However, in regions with intense competition for iron, some microbes optimize iron acquisition by producing siderophores that minimize diffusive losses to the environment. These siderophores affect iron bioavailability and thus may be an important component of the marine iron cycle.

Significance Oceanic dissolved organic carbon (DOC) contains as much carbon as Earth’s atmosphere, yet its cycling timescales and composition remain poorly constrained. We use serial oxidation experiments to measure the quantitative distribution of carbon isotopes inside the DOC reservoir, allowing us to estimate both its cycling timescales and source distribution. We find that a large portion of deep water DOC has a modern radiocarbon age and a fast turnover time supported by particle dissolution. In addition, stable carbon isotopes allow for diverse sources of carbon, besides microbial production, to quantitatively feed this reservoir. Our work suggests a DOC cycle that is far more intricate, and potentially variable on shorter timescales, than previously envisioned. Marine dissolved organic carbon (DOC) is a large (660 Pg C) reactive carbon reservoir that mediates the oceanic microbial food web and interacts with climate on both short and long timescales. Carbon isotopic content provides information on the DOC source via δ ¹³C and age via Δ ¹⁴C. Bulk isotope measurements suggest a microbially sourced DOC reservoir with two distinct components of differing radiocarbon age. However, such measurements cannot determine internal dynamics and fluxes. Here we analyze serial oxidation experiments to quantify the isotopic diversity of DOC at an oligotrophic site in the central Pacific Ocean. Our results show diversity in both stable and radio isotopes at all depths, confirming DOC cycling hidden within bulk analyses. We confirm the presence of isotopically enriched, modern DOC cocycling with an isotopically depleted older fraction in the upper ocean. However, our results show that up to 30% of the deep DOC reservoir is modern and supported by a 1 Pg/y carbon flux, which is 10 times higher than inferred from bulk isotope measurements. Isotopically depleted material turns over at an apparent time scale of 30,000 y, which is far slower than indicated by bulk isotope measurements. These results are consistent with global DOC measurements and explain both the fluctuations in deep DOC concentration and the anomalous radiocarbon values of DOC in the Southern Ocean. Collectively these results provide an unprecedented view of the ways in which DOC moves through the marine carbon cycle.

Dissolved organic matter (DOM) in the oceans is one of the largest pools of reduced carbon on Earth, comparable in size to the atmospheric CO ₂ reservoir. A vast number of compounds are present in DOM, and they play important roles in all major element cycles, contribute to the storage of atmospheric CO ₂ in the ocean, support marine ecosystems, and facilitate interactions between organisms. At the heart of the DOM cycle lie molecular-level relationships between the individual compounds in DOM and the members of the ocean microbiome that produce and consume them. In the past, these connections have eluded clear definition because of the sheer numerical complexity of both DOM molecules and microorganisms. Emerging tools in analytical chemistry, microbiology, and informatics are breaking down the barriers to a fuller appreciation of these connections. Here we highlight questions being addressed using recent methodological and technological developments in those fields and consider how these advances are transforming our understanding of some of the most important reactions of the marine carbon cycle.

Marine dissolved organic matter (DOM) contains as much carbon as the Earth's atmosphere, and represents a critical component of the global carbon cycle. To better define microbial processes and activities associated with marine DOM cycling, we analyzed genomic and transcriptional responses of microbial communities to high-molecular-weight DOM (HMWDOM) addition. The cell density in the unamended control remained constant, with very few transcript categories exhibiting significant differences over time. In contrast, the DOM-amended microcosm doubled in cell numbers over 27 h, and a variety of HMWDOM-stimulated transcripts from different taxa were observed at all time points measured relative to the control. Transcripts significantly enriched in the HMWDOM treatment included those associated with two-component sensor systems, phosphate and nitrogen assimilation, chemotaxis, and motility. Transcripts from Idiomarina and Alteromonas spp., the most highly represented taxa at the early time points, included those encoding TonB-associated transporters, nitrogen assimilation genes, fatty acid catabolism genes, and TCA cycle enzymes. At the final time point, Methylophaga rRNA and non-rRNA transcripts dominated the HMWDOM-amended microcosm, and included gene transcripts associated with both assimilatory and dissimilatory single-carbon compound utilization. The data indicated specific resource partitioning of DOM by different bacterial species, which results in a temporal succession of taxa, metabolic pathways, and chemical transformations associated with HMWDOM turnover. These findings suggest that coordinated, cooperative activities of a variety of bacterial \"specialists\" may be critical in the cycling of marine DOM, emphasizing the importance of microbial community dynamics in the global carbon cycle.

River inputs of nutrients and organic matter impact the biogeochemistry of arctic estuaries and the Arctic Ocean as a whole, yet there is considerable uncertainty about the magnitude of fluvial fluxes at the pan-Arctic scale. Samples from the six largest arctic rivers, with a combined watershed area of 11.3 x 10⁶ km², have revealed strong seasonal variations in constituent concentrations and fluxes within rivers as well as large differences among the rivers. Specifically, we investigate fluxes of dissolved organic carbon, dissolved organic nitrogen, total dissolved phosphorus, dissolved inorganic nitrogen, nitrate, and silica. This is the first time that seasonal and annual constituent fluxes have been determined using consistent sampling and analytical methods at the pan-Arctic scale and consequently provide the best available estimates for constituent flux from land to the Arctic Ocean and surrounding seas. Given the large inputs of river water to the relatively small Arctic Ocean and the dramatic impacts that climate change is having in the Arctic, it is particularly urgent that we establish the contemporary river fluxes so that we will be able to detect future changes and evaluate the impact of the changes on the biogeochemistry of the receiving coastal and ocean systems.

Sunlight is the dominant control on phytoplankton biosynthetic activity, and darkness deprives them of their primary external energy source. Changes in the biochemical composition of phytoplankton communities over diel light cycles and attendant consequences for carbon and energy flux in environments remain poorly elucidated. Here we use lipidomic data from the North Pacific subtropical gyre to show that biosynthesis of energy-rich triacylglycerols (TAGs) by eukaryotic nanophytoplankton during the day and their subsequent consumption at night drives a large and previously uncharacterized daily carbon cycle. Diel oscillations in TAG concentration comprise 23 ± 11% of primary production by eukaryotic nanophytoplankton representing a global flux of about 2.4 Pg C yr −1 . Metatranscriptomic analyses of genes required for TAG biosynthesis indicate that haptophytes and dinoflagellates are active members in TAG production. Estimates suggest that these organisms could contain as much as 40% more calories at sunset than at sunrise due to TAG production. Day-night cycles in the biochemical composition of phytoplankton remain poorly understood. Here, Becker et al. use lipidomic and transcriptomic data from the North Pacific subtropical gyre to describe a daily cycle of production and consumption of energy-rich lipids by eukaryotic phytoplankton.

Picophytoplankton, including photosynthetic picoeukaryotes (PPE) and unicellular cyanobacteria, are important contributors to plankton biomass and primary productivity. In this study, phytoplankton composition and rates of carbon fixation were examined across a large trophic gradient in the South East Pacific Ocean (SEP) using a suite of approaches: photosynthetic pigments, rates of 14C-primary productivity, and phylogenetic analyses of partial 18S rRNA genes PCR amplified and sequenced from flow cytometrically sorted cells. While phytoplankton > 10 μm (diatoms and dinoflagellates) were prevalent in the upwelling region off the Chilean coast, picophytoplankton consistently accounted for 55–92% of the total chlorophyll a inventories and > 60% of 14C-primary productivity throughout the sampling region. Estimates of rates of 14C-primary productivity derived from flow cytometric sorting of radiolabeled cells revealed that the contributions of PPE and Prochlorococcus to euphotic zone depth-integrated picoplankton productivity were nearly equivalent (ranging 36–57%) along the transect, with PPE comprising a larger share of picoplankton productivity than cyanobacteria in the well-lit (> 15% surface irradiance) region compared with in the lower regions (1–7% surface irradiance) of the euphotic zone. 18S rRNA gene sequence analyses revealed the taxonomic identities of PPE; e.g., Mamiellophyceae (Ostreococcus) were the dominant PPE in the upwelling-influenced waters, while members of the Chrysophyceae, Prymnesiophyceae, Pelagophyceae, and Prasinophyceae Clades VII and IX flourished in the oligotrophic South Pacific Subtropical Gyre. Our results suggest that, despite low numerical abundance in comparison to cyanobacteria, diverse members of PPE are significant contributors to carbon cycling across biogeochemically distinct regions of the SEP.

The role of bacterioplankton in the cycling of marine dissolved organic matter (DOM) is central to the carbon and energy balance in the ocean, yet there are few model organisms available to investigate the genes, metabolic pathways, and biochemical mechanisms involved in the degradation of this globally important carbon pool. To obtain microbial isolates capable of degrading semi-labile DOM for growth, we conducted dilution to extinction cultivation experiments using seawater enriched with high molecular weight (HMW) DOM. In total, 93 isolates were obtained. Amendments using HMW DOM to increase the dissolved organic carbon concentration 4x (280 μ M ) or 10x (700 μ M ) the ocean surface water concentrations yielded positive growth in 4–6% of replicate dilutions, whereas <1% scored positive for growth in non-DOM-amended controls. The majority (71%) of isolates displayed a distinct increase in cell yields when grown in increasing concentrations of HMW DOM. Whole-genome sequencing was used to screen the culture collection for purity and to determine the phylogenetic identity of the isolates. Eleven percent of the isolates belonged to the gammaproteobacteria including Alteromonadales (the SAR92 clade) and Vibrio . Surprisingly, 85% of isolates belonged to the methylotrophic OM43 clade of betaproteobacteria, bacteria thought to metabolically specialize in degrading C1 compounds. Growth of these isolates on methanol confirmed their methylotrophic phenotype. Our results indicate that dilution to extinction cultivation enriched with natural sources of organic substrates has a potential to reveal the previously unsuspected relationships between naturally occurring organic nutrients and the microorganisms that consume them.