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Microbial decomposition of marine dissolved organic matter in cool oceanic crust

Abstract

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.

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Fig. 1: Sampling locations and schematic representation of the DOC transformation within the crust at the North Pond IODP study site.
Fig. 2: Concentrations of dissolved oxygen and DOC with SPE-DOM molecular composition indices versus incubation time in the North Pond crustal aquifer.
Fig. 3: Isotopic composition of bottom water and crustal DIC and DOC at North Pond.

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Acknowledgements

We thank the captain and crew of the RV Maria S. Merian, the pilots and engineers of the ROV Jason II and W. Bach, K. Edwards, B. Orcutt, G. Wheat, B. Glazer, J. Meyer, H.-T. Lin, and C.-C. Hsieh for their work in accomplishing the field programmes, as well as A. McNichol and the staff of the sample preparation lab at NOSAMS. We owe a special thanks to B. Kraft for sampling fluids for us in 2014. Ship time was provided by the German Science Foundation. Bathymetry data were provided by H. Villinger. D. Repeta provided critical insight into the nature and isotopic composition of marine DOC, which improved our manuscript. It also benefitted from discussions with G. Wheat and J. Mikucki. This work was supported by NSF OCE-1061934 and NSF-1542506 to P.R.G., NSF OCE-1062006 and OCE-1635208 to J.A.H., NSF OCE-1635365 to S.R.S.W. and P.R.G., and NSF OCE-1260408 and OCE-1355870 to A.T.F. S.R.S.W. was also supported by the WHOI Postdoctoral Scholar Program and the NSF Cooperative Agreement for the Operation of a NOSAMS Facility (OCE-075348). The Center for Dark Energy Biosphere Investigations (C-DEBI (OCE-0939564)) supported the participation of J.A.H. and A.T.F., as well as U.J., through a C-DEBI Postdoctoral Fellowship. The Gordon and Betty Moore Foundation provided additional support to A.P. This is C-DEBI contribution number 413.

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S.R.S.W., U.J., P.R.G. and J.A.H. formulated the original hypotheses and designed the project, S.R.S.W., U.J., H.O., T.D. and P.R.G. collected samples, performed research and participated in the data analysis and data interpretation. A.T.F. provided fluid-flow calculations and constraints. All the authors discussed the data presented in this manuscript and participated in its writing.

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Correspondence to Sunita R. Shah Walter or Peter R. Girguis.

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Shah Walter, S.R., Jaekel, U., Osterholz, H. et al. Microbial decomposition of marine dissolved organic matter in cool oceanic crust. Nature Geosci 11, 334–339 (2018). https://doi.org/10.1038/s41561-018-0109-5

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