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 splendidus 1A01; Pseudoalteromonas sp. 3D05). Continuous measurement of respiratory CO2 production and its carbon isotopic compositions (13C and 14C) shows species‐specific differences in the rate, quantity, and type of organic matter remineralized. Each species was incubated with hydrothermally‐influenced vs. unimpacted sediments, resulting in a ~2‐fold difference in respiratory CO2 yield 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.
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.
Aquatic sediments harbor diverse microbial communities that mediate organic matter degradation and influence biogeochemical cycles. The pool of bioavailable carbon continuously changes as a result of abiotic processes and microbial activity. It remains unclear how microbial communities respond to heterogeneous organic matrices and how this ultimately affects heterotrophic respiration. To explore the relationships between the degradation of mixed carbon substrates and microbial activity, we incubated batches of organic-rich sediments in a novel bioreactor (IsoCaRB) that permitted continuous observations of CO2 production rates, as well as sequential sampling of isotopic signatures (δ13C, Δ14C), microbial community structure and diversity, and extracellular enzyme activity. Our results indicated that lower molecular weight (MW), labile, phytoplankton-derived compounds were degraded first, followed by petroleum-derived exogenous pollutants, and finally by higher MW polymeric plant material. This shift in utilization coincided with a community succession and increased extracellular enzyme activities. Thus, sequential utilization of different carbon pools induced changes at both the community and cellular level, shifting community composition, enzyme activity, respiration rates, and residual organic matter reactivity. Our results provide novel insight into the accessibility of sedimentary organic matter and demonstrate how bioavailability of natural organic substrates may affect the function and composition of heterotrophic bacterial populations. This article is protected by copyright. All rights reserved.
The biogeochemical transformation and remineralization of organic matter (OM) in marine sediments is largely driven by the activity of complex and diverse microbial communities. A major unknown in carbon biogeochemistry is determining what controls the reactivity or lability of OM to microorganisms. Recent studies have found that the ability to use different carbon sources varies among microorganisms, suggesting that the reactivity of specific carbon pools can be specific to the taxa that utilize the pool. This project investigated the extent to which the reactivity and transformation of OM is species-specific. Using a novel bioreactor system (IsoCaRB), we carried out time-series incubations using bacterial isolates and sterilized organic-rich sediment collected from Guaymas Basin. The IsoCaRB system allows us to measure the production rate and natural isotopic (Δ14C and δ13C) signature of microbially-respired CO2 to constrain the type and age of organic matter that is accessible to each species. Separate incubations using marine bacterial isolates (Vibrio sp. and Pseudoalteromonas sp.) and sterilized sediment under oxic conditions showed that the rate and total quantity of organic matter metabolized by these two species differs. Approximately twice as much respired CO2 was collected during the Pseudoalteromonas sp. incubations compared to the Vibrio sp. incubations. Δ14C and δ13C signatures of respired CO2 show selective utilization of different carbon pools by the two species. These differences in OM degradation may be due to the gene copy number and substrate specificity of degradative enzymes. The results of this work indicate that organic matter transformation in marine sediments may depend on the metabolic capabilities of the microbial populations that are present and active.