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Abstract 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. 

Microorganisms that transform and oxidize organic material (that is, heterotrophs) play a fundamental role in the geochemical cycling of key elements in the ocean. Through their growth and activity, heterotrophic microorganisms degrade much of the organic matter produced by phytoplankton in the surface ocean, leading to the regeneration and redistribution of nutrients and carbon back into the water column. However, most organic matter is physically too large to be taken up directly by heterotrophic microorganisms. Consequently, many heterotrophs secrete exoenzymes that break down large molecules outside the cell into smaller substrates that can then be directly taken up by the cell. The complex nature of the biochemical systems that microorganisms use to secrete these enzymes suggests that they were unlikely to have been present in the earliest heterotrophs. In a pre-exoenzyme ocean, heterotrophic microorganisms would only be able to access a small fraction of organic matter such that most dead phytoplankton biomass would have passed directly through the water column and settled onto the seafloor. Here we synthesize existing geobiological evidence to examine the fate of organic matter in the absence of exoenzymes in early oceans. We propose that on an Earth before exoenzymes, organic matter preservation, metal availability and phosphorus recycling would have operated differently than they do on the contemporary Earth. 

Summary Marine microorganisms play a fundamental role in the global carbon cycle by mediating the sequestration of organic matter in ocean waters and sediments. A better understanding of how biological factors, such as microbial community composition, influence the lability and fate of organic matter is needed. Here, we explored the extent to which organic matter remineralization is influenced by species‐specific metabolic capabilities. We carried out aerobic time‐series incubations of Guaymas Basin sediments to quantify the dynamics of carbon utilization by two different heterotrophic marine isolates (Vibrio splendidus1A01;Pseudoalteromonassp. 3D05). Continuous measurement of respiratory CO₂production and its carbon isotopic compositions (¹³C and¹⁴C) shows species‐specific differences in the rate, quantity and type of organic matter remineralized. Each species was incubated with hydrothermally‐influenced versus unimpacted sediments, resulting in a ~2‐fold difference in respiratory CO₂yield across the experiments. Genomic analysis indicated that the observed carbon utilization patterns may be attributed in part to the number of gene copies encoding for extracellular hydrolytic enzymes. Our results demonstrate that the lability and remineralization of organic matter in marine environments is not only a function of chemical composition and/or environmental conditions, but also a function of the microorganisms that are present and active.