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Marine dissolved organic carbon (DOC) is one of the largest active reservoirs of reduced carbon on Earth. In the deep ocean, DOC has been described as biologically recalcitrant and has a radiocarbon age of 4,000 to 6,000 years, which far exceeds the timescale of ocean overturning. However, abiotic removal mechanisms cannot account for the full magnitude of deep-ocean DOC loss. Deep-ocean water circulates at low temperatures through volcanic crust on ridge flanks, but little is known about the associated biogeochemical processes and carbon cycling. Here we present analyses of DOC in fluids from two borehole observatories installed in crustal rocks west of the Mid-Atlantic Ridge, and show that deep-ocean DOC is removed from these cool circulating fluids. The removal mechanism is isotopically selective and causes a shift in specific features of molecular composition, consistent with microbe-mediated oxidation. We suggest organic molecules with an average radiocarbon age of 3,200 years are bioavailable to crustal microbes, and that this removal mechanism may account for at least 5% of the global loss of DOC in the deep ocean. Cool crustal circulation probably contributes to maintaining the deep ocean as a reservoir of ‘aged’ and refractory DOC by discharging the surviving organic carbon constituents that are molecularly degraded and depleted in 14C and 13C into the deep ocean.

Salt marshes can emit significant methane to the atmosphere. These emissions are highly variable, but the cause of this variability is not well understood. Although methanogenesis should be inhibited by sulfate reduction where sulfate is present due to its thermodynamic unfavorableness, methane emissions are not well predicted by sulfate concentrations; thus, other controls on methane production must be active. One hypothesis is that where sulfate is present, salt marsh methanogens are fueled by methylated carbon substrates that sulfate reducers do not compete for. It has also been shown that crystalline iron minerals can facilitate increased methane production in low-salinity wetlands, but this has not been explored in salt marshes. This study documents how different organic carbon sources (monomethylamine and ethanol) and Fe(III) minerals (ferrihydrite, magnetite, and hematite) influence methane production by microbial communities from a polyhaline tidal marsh creek in the Great Marsh Preserve, DE, USA. Carbon source had a strong influence on microbial community composition by the end of the incubations. More methane was produced with monomethylamine amendment than with ethanol, and the highest methane production rates were in incubations supplied with both monomethylamine and magnetite or hematite. This increased methane production in the presence of (semi)conductive iron minerals could indicate that interspecies electron transfer was active in some of our treatments. However, instead of the more commonly described syntrophic partners, this interaction appears to be between methylotrophic methanogens belonging to Methanococcoides and an unidentified iron-reducing bacterial group, possibly Candidatus Omnitrophus. Much less methane was measured with ethanol and ferrihydrite amendments. However, in ethanol-amended incubations, a small proportion of anaerobic methane oxidizers was detected, which suggests that both methane production and re-oxidation may have occurred, leading to low measured methane production. Although some iron reduction and Fe2+ production was observed in all treatments, significant transformation of ferrihydrite to magnetite was observed only with ethanol amendment. If microbially mediated magnetite formation occurs in salt marsh sediment, our observations indicate that the resulting magnetite could enhance methane production by methylotrophic methanogens. This study highlights the importance of methylated compounds to salt marsh methane production as well as the potential importance of iron mineral composition for predicting methane production and iron reduction rates.

Growing evidence suggests that interactions among heterotrophic microorganisms influence the efficiency and rate of organic matter turnover. These interactions are dynamic and shaped by the composition and availability of resources in their surrounding environment. Heterotrophic microorganisms inhabiting marine environments often encounter fluctuations in the quality and quantity of carbon inputs, ranging from simple sugars to large, complex compounds. Here, we experimentally tested how the chemical complexity of carbon substrates affects competition and growth dynamics between two heterotrophic marine isolates. We tracked cell density using species-specific polymerase chain reaction (PCR) assays and measured rates of microbial CO2 production along with associated isotopic signatures (13C and 14C) to quantify the impact of these interactions on organic matter remineralization. The observed cell densities revealed substrate-driven interactions: one species exhibited a competitive advantage and quickly outgrew the other when incubated with a labile compound whereas both species seemed to coexist harmoniously in the presence of more complex organic matter. Rates of CO2 respiration revealed that coincubation of these isolates enhanced organic matter turnover, sometimes by nearly 2-fold, compared to their incubation as mono-cultures. Isotopic signatures of respired CO2 indicated that coincubation resulted in a greater remineralization of macromolecular organic matter. These results demonstrate that simple substrates promote competition whereas high substrate complexity reduces competitiveness and promotes the partitioning of degradative activities into distinct niches, facilitating coordinated utilization of the carbon pool. Taken together, this study yields new insight into how the quality of organic matter plays a pivotal role in determining microbial interactions within marine environments.

A substantial fraction of marine sediments experience elevated temperatures due to burial or hydrothermal activity. These conditions can fundamentally reshape both microbial activity and the chemical nature of sedimentary organic matter (OM). Laboratory incubations have demonstrated that moderate heating of marine sediments can lead to the production of labile organic compounds such as acetate, however, it remains unclear whether heating alters the bioavailability of the remaining OM pool. In this study, we experimentally tested the effect of temperature on the bioavailability of OM through a series of bioreactor experiments using deeply buried sediment collected from Guaymas Basin (Gulf of California). We measured acetate concentrations in sterilized Guaymas Basin sediments before and after artificial heating (70°C for 7 days) to quantify abiotic acetate generation. We then conducted incubations of a model marine bacterium with sterilized, artificially heated sediment and tracked respired CO2 production and its associated 13C and 14C signatures. Our study revealed that sediment depth and hydrothermal history strongly control abiotic acetate production, with higher acetate yields from shallower, cooler sediments. Respiration rates in control and heated sediment incubations were nearly identical, indicating that heating does not measurably alter the bioavailability of bulk sedimentary OM. Moreover, the δ13C values of respired CO2 were indistinguishable between control and heated sediment incubations while the Δ14C values were more depleted in the first 24 hours in incubations with heated sediment. This transient offset suggests that low-temperature heating mobilizes a small pool of older material due to desorption of mineral-bound OM without altering overall bioavailability. Our findings shed light on the role of thermal alteration in shaping carbon cycling in marine sediments by influencing how OM is made available to sedimentary microorganisms.

Growing evidence suggests that interactions among heterotrophic microbes influence the efficiency and rate of organic matter turnover. These interactions are dynamic and shaped by the composition and availability of resources in their surrounding environment. Heterotrophic microbes inhabiting marine environments often encounter fluctuations in the quality and quantity of carbon inputs, ranging from simple sugars to large, complex compounds. Here, we experimentally tested how the chemical complexity of carbon substrates affects competition and growth dynamics between two heterotrophic marine isolates. We tracked cell density using species-specific PCR assays and measured rates of microbial CO2 production along with associated isotopic signatures (13C and 14C) to quantify the impact of these interactions on organic matter remineralization. The observed cell densities revealed substrate-driven interactions: one species exhibited a competitive advantage and quickly outgrew the other when incubated with a labile compound while both species seemed to coexist harmoniously in the presence of more complex organic matter. Rates of CO2 respiration revealed that co-incubation of these isolates enhanced organic matter turnover, sometimes by nearly twofold, compared to their incubation as mono-cultures. Isotopic signatures of respired CO2 indicated that co-incubation resulted in a greater remineralization of macromolecular organic matter. These results demonstrate that simple substrates promote competition while high substrate complexity reduces competitiveness and promotes the partitioning of degradative activities into distinct niches, facilitating coordinated utilization of the carbon pool. Taken together, this study yields new insight into how the quality of organic matter plays a pivotal role in determining microbial interactions within marine environments.