Abstract
Marine organic matter is one of Earth’s largest actively cycling reservoirs of organic carbon and nitrogen1,2. The processes controlling organic matter production and removal are important for carbon and nitrogen biogeochemical cycles, which regulate climate. However, the many possible cycling mechanisms have hindered our ability to quantify marine organic matter transformation, degradation and turnover rates3,4. Here we analyse existing and new measurements of the carbon:nitrogen ratio and radiocarbon age of organic matter spanning sizes from large particulate organic matter to small dissolved organic molecules. We find that organic matter size is negatively correlated with radiocarbon age and carbon:nitrogen ratios in coastal, surface and deep waters of the Pacific Ocean. Our measurements suggest that organic matter is increasingly chemically degraded as it decreases in size, and that small particles and molecules persist in the ocean longer than their larger counterparts. Based on these correlations, we estimate the production rates of small, biologically recalcitrant dissolved organic matter molecules at 0.11–0.14 Gt of carbon and about 0.005 Gt of nitrogen per year in the deep ocean. Our results suggest that the preferential remineralization of large over small particles and molecules is a key process governing organic matter cycling and deep ocean carbon storage.
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References
Hansell, D. A. Relcalcitrant dissolved organic carbon fractions. Ann. Rev. Mar. Sci. 5, 421–445 (2013).
Jiao, N. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599 (2010).
Carlson, C. A. in Biogeochemistry of Marine Dissolved Organic Matter (eds Hansell, D. A & Carlson, C. A) 91–151 (Academic, 2002).
Lee, C., Wakeham, S. & Arnosti, C. Particulate organic matter in the sea: the composition conundrum. Ambio 33, 565–575 (2004).
McNichol, A. P. & Aluwihare, L. I. The power of radiocarbon in biogeochemical studies of the marine carbon cycle: insights from studies of dissolved and particulate organic carbon (DOC and POC). Chem. Rev. 107, 443–466 (2007).
Williams, P. M. & Druffel, E. R. M. Radiocarbon in dissolved organic-matter in the central north pacific-ocean. Nature 330, 246–248 (1987).
Beaupre, S. R. & Druffel, E. R. M. Constraining the propagation of bomb-radiocarbon through the dissolved organic carbon (DOC) pool in the northeast Pacific Ocean. Deep-Sea Res. I 56, 1717–1726 (2009).
Druffel, E. R. M. & Williams, P. M. Identification of a deep marine source of particulate organic-carbon using bomb C-14. Nature 347, 172–174 (1990).
Benner, R. & Amon, R. M. W. The size–reactivity continuum of major bioelements in the ocean. Ann. Rev. Mar. Sci. 7, 185–205 (2015).
Walker, B. D., Beaupre, S. R., Guilderson, T. P., Druffel, E.R.M. & McCarthy, M. D. Large-volume ultrafiltration for the study of radiocarbon signatures and size vs. age relationships in marine dissolved organic matter. Geochim. Cosmochim. Acta 75, 5187–5202 (2011).
Amon, R. M. W. & Benner, R. Bacterial utilization of different size classes of dissolved organic matter. Limnol. Oceanogr. 41, 41–51 (1996).
Benner, R. & Herndl, G. J. in Microbial Carbon Pump in the Ocean (eds Jiao, N., Azam, F. & Sanders, S.) 46–48 (Science AAAS, 2011).
Brophy, J. E. & Carlson, D. J. Production of biologically refractory dissolved organic carbon by natural seawater microbial populations. Deep-Sea Res. 36, 497–507 (1989).
Walker, B. D., Guilderson, T. P., Okimura, K. M., Peacock, M. B. & McCarthy, M. D. Radiocarbon signatures and size–age–composition relationships of major organic matter pools within a unique California upwelling system. Geochim. Cosmochim. Acta 126, 1–17 (2014).
Walker, B. D. & McCarthy, M. D. Elemental and isotopic characterization of dissolved and particulate organic matter in a unique California upwelling system: importance of size and composition in the export of labile material. Limnol. Oceanogr. 57, 1757–1774 (2012).
Benner, R. in Biogeochemistry of Marine Dissolved Organic Matter (eds Hansell, D. A. & Carlson, C. A.) 59–90 (Academic, 2002).
Smith, D. C., Simon, M., Alldredge, A. L. & Azam, F. Intense hydrolytic enzyme activity on marine aggregates and implications for rapide particle dissolution. Nature 359, 139–142 (1992).
Middelburg, J. J. Chemoautotrophy in the ocean. Geophys. Res. Lett. 38, L24604 (2011).
Ingalls, A. E. et al. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc. Natl Acad. Sci. USA 103, 6442–6447 (2006).
Rau, G. H. Another recipe for bomb C-14 dilution. Nature 350, 116 (1991).
Verdugo, P. Marine microgels. Ann. Rev. Mar. Sci. 4, 375–400 (2012).
Babbin, A. R., Keil, R. G., Devol, A. H. & Ward, B. B. Organic matter stoichiometry, flux, and oxygen control nitrogen loss in the ocean. Science 344, 406–408 (2014).
McCarthy, M. D. et al. Chemosynthetic origin of 14C-depleted dissolved organic matter in a ridge-flank hydrothermal system. Nat. Geosci. 4, 32–36 (2011).
Muller-Karger, F. E. et al. The importance of continental margins in the global carbon cycle. Geophys. Res. Lett. 32, L01602 (2005).
Pohlman, J. W., Bauer, J. E., Waite, W. F., Osburn, C. L. & Chapman, N. R. Methane hydrate-bearing seeps as a source of aged dissolved organic carbon to the oceans. Nat. Geosci. 4, 37–41 (2011).
Feely, R. A. et al. Oxygen utilization and organic carbon remineralization in the upper water column of the Pacific Ocean. J. Oceanogr. 60, 45–52 (2004).
Emerson, S. Annual net community production and the biological carbon flux in the ocean. Glob. Biogeochem. Cycles 28, 14–28 (2014).
Druffel, E. R. M. & Griffin, S. Radiocarbon in dissolved organic carbon of the South Pacific Ocean. Geophys. Res. Lett. 42, 4096–4101 (2015).
Bauer, J. E. & Druffel, E. R. M. Ocean margins as a significant source of organic matter to the deep open ocean. Nature 392, 482–485 (1998).
Arrieta, J. M. et al. Dilution limits dissolved organic carbon utilization in the deep ocean. Science 348, 331–333 (2015).
Reeburgh, W. S. Figures summarizing the global cycles of biogeochemically important elements. Bull. Ecol. Soc. Am. 78, 260–267 (1997).
Roland, L. A., McCarthy, M. D., Peterson, T. D. & Walker, B. D. A large-volume micro-filtration system for isolating suspended particulate organic matter: fabrication and assessment vs. GFF filters in central N. Pacific. Limnol. Oceanogr. 7, 64–80 (2009).
Vogel, J. S., Southon, J. R. & Nelson, D. E. Catalyst and binder effects in the use of filamentous graphite for Ams. Nucl. Instr. Meth. Phys. Res. B 29, 50–56 (1987).
Beaupre, S. R., Druffel, E. R. M. & Griffin, S. A low-blank photochemical extraction system for concentration and isotopic analyses of marine dissolved organic carbon. Limnol. Oceanogr. 5, 174–184 (2007).
Stuiver, M. & Polach, H. A. Discussion: reporting of 14C data. Radiocarbon 19, 355–363 (1977).
Sheldon, R. W., Prakash, A. & Sutcliff, W. H. Jr Size distribution of particles in the ocean. Limnol. Oceanogr. 17, 327–340 (1972).
Chisholm, S. W. Phytoplankton size. Environ. Sci. Res. 43, 213–237 (1992).
Hertkorn, N. et al. Characterization of a major refractory component of marine dissolved organic matter. Geochim. Cosmochim. Acta 70, 2990–3010 (2006).
D’Andrilli, J. et al. Comprehensive characterization of marine dissolved organic matter by Fourier transform ion cyclotron resonance mass spectrometry with electrospray and atmospheric pressure photoionization. Rapid Commun. Mass Spectrom. 24, 643–650 (2010).
Dittmar, T. & Kattner, G. Recalcitrant dissolved organic matter in the ocean: major contribution of small amphiphilics. Mar. Chem. 82, 115–123 (2003).
Repeta, D. J. & Aluwihare, L. I. Radiocarbon analysis of neutral sugars in high-molecular-weight dissolved organic carbon: Implications for organic carbon cycling. Limnol. Oceanogr. 51, 1045–1053 (2006).
Toggweiler, J. R., Dixon, K. & Bryan, K. Simulations of radiocarbon in a coarse-resolution world ocean model 1. Steady-state prebomb distributions. J. Geophys. Res. 94, 8217–8242 (1989).
Masiello, C. A., Druffel, E. R. M. & Bauer, J. E. Physical controls on dissolved inorganic radiocarbon variability in the California current. Deep-Sea Res. II 45, 617–642 (1998).
Acknowledgements
We gratefully acknowledge B. Phillips, the staff of the Granite Canyon Marine Pollution Studies Laboratory (GCMPSL) and the Natural Energy Laboratory of Hawaii Authority (NELHA) for providing facilities capable of large-volume seawater DOM and suspended POM isolations. K. Okimura, J. Walker, L. Roland, K. Walker, G. V. Reixach, and M. Calleja (UC Santa Cruz) aided with fieldwork and sample collection. S. Griffin (UCI) and P. Zermeno (LLNL) aided with sample analysis. F. Primeau (UCI) aided with error analysis and Matlab scripts. This work was funded by the Friends of Long Marine Lab Student Research Awards (to B.D.W.), the UC Santa Cruz STEPS Institute for Innovation in Environmental Research (to B.D.W.), the UC Santa Cruz Center for the Dynamics and Evolution of the Land-Sea Interface (to B.D.W.), the Earl H. Myers and Ethel M. Myers Oceanographic and Marine Biology Trust (to B.D.W.), the UC Santa Cruz Institute of Geophysics and Planetary Physics (to B.D.W. and M.D.M.), NSF OCE-1358041 and NSF OCE-0623622 (M.D.M.) and NSF ARC-1022716 (E.R.M.D.). A portion of this work was performed under the auspices of the US Department of Energy (contract W-7405-Eng-48 and DE-AC52-07NA27344) and a Keck Carbon Cycle AMS Laboratory Postdoctoral Scholarship (B.D.W.).
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B.D.W. conceived the research; B.D.W., S.R.B., T.P.G., M.D.M. and E.R.M.D. performed research; S.R.B., T.P.G., and E.R.M.D. contributed new reagents/analytical tools and models; B.D.W., S.R.B., T.P.G., E.R.M.D. and M.D.M. analysed data; B.D.W. wrote the paper with inputs from S.R.B., T.P.G., M.D.M. and E.R.M.D.
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Walker, B., Beaupré, S., Guilderson, T. et al. Pacific carbon cycling constrained by organic matter size, age and composition relationships. Nature Geosci 9, 888–891 (2016). https://doi.org/10.1038/ngeo2830
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DOI: https://doi.org/10.1038/ngeo2830
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