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Global niche of marine anaerobic metabolisms expanded by particle microenvironments

Abstract

In ocean waters, anaerobic microbial respiration should be confined to the anoxic waters found in coastal regions and tropical oxygen minimum zones, where it is energetically favourable. However, recent molecular and geochemical evidence has pointed to a much broader distribution of denitrifying and sulfate-reducing microbes. Anaerobic metabolisms are thought to thrive in microenvironments that develop inside sinking organic aggregates, but the global distribution and geochemical significance of these microenvironments is poorly understood. Here, we develop a new size-resolved particle model to predict anaerobic respiration from aggregate properties and seawater chemistry. Constrained by observations of the size spectrum of sinking particles, the model predicts that denitrification and sulfate reduction can be sustained throughout vast, hypoxic expanses of the ocean, and could explain the trace metal enrichment observed in particles due to sulfide precipitation. Globally, the expansion of the anaerobic niche due to particle microenvironments doubles the rate of water column denitrification compared with estimates based on anoxic zones alone, and changes the sensitivity of the marine nitrogen cycle to deoxygenation in a warming climate.

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Fig. 1: Particle size spectrum and microenvironment model schematic.
Fig. 2: Predicted microenvironment distributions at two sites in the tropical ocean.
Fig. 3: Microenvironment-driven accumulation of trace metals in the tropical North Atlantic.
Fig. 4: Expanded niche of anaerobic metabolism in the ocean.
Fig. 5: Sensitivity of particle denitrification to climate-forced oxygen trends.

References

  1. 1.

    Thamdrup, B., Dalsgaard, T. & Peter Revsbech, N. Widespread functional anoxia in the oxygen minimum zone of the eastern South Pacific. Deep Sea Res. Pt I 65, 36–45 (2012).

    Article  Google Scholar 

  2. 2.

    Froelich, P. N. et al. Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim. Cosmochim. Acta 43, 1075–1090 (1979).

    Article  Google Scholar 

  3. 3.

    Garcia, H. E. et al. World Ocean Atlas 2009, Volume 4: Nutrients (Phosphate, Nitrate, and Silicate) NOAA Atlas NESDIS 71 (U.S. Government Printing Office, Washington, DC, 2010).

  4. 4.

    Ulloa, O., Canfield, D. E., DeLong, E. F., Letelier, R. M. & Stewart, F. J. Microbial oceanography of anoxic oxygen minimum zones. Proc. Natl Acad. Sci. USA 109, 15996–16003 (2012).

    Article  Google Scholar 

  5. 5.

    Smith, M. W., Allen, L. Z., Allen, A. E., Herfort, L. & Simon, H. M. Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem. Front. Microbiol. 4, 120 (2013).

    Google Scholar 

  6. 6.

    Ganesh, S., Parris, D. J., DeLong, E. F. & Stewart, F. J. Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone. ISME J. 8, 187–211 (2014).

    Article  Google Scholar 

  7. 7.

    Michotey, V. & Bonin, P. Evidence for anaerobic bacterial processes in the water column: denitrification and dissimilatory nitrate ammonification in the northwestern Mediterranean Sea. Mar. Ecol. Progress. Ser. 160, 47–56 (1997).

    Article  Google Scholar 

  8. 8.

    Wolgast, D., Carlucci, A. & Bauer, J. Nitrate respiration associated with detrital aggregates in aerobic bottom waters of the abyssal NE Pacific. Deep Sea Res. Pt II 45, 881–892 (1998).

    Article  Google Scholar 

  9. 9.

    Kalvelage, T. et al. Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones. PLoS ONE 6, e29299 (2011).

    Article  Google Scholar 

  10. 10.

    Fuchs, B. M., Woebken, D., Zubkov, M. V., Burkill, P. & Amann, R. Molecular identification of picoplankton populations in contrasting waters of the Arabian Sea. Aquat. Microb. Ecol. 39, 145–157 (2005).

    Article  Google Scholar 

  11. 11.

    Canfield, D. E. et al. A cryptic sulfur cycle in oxygen-minimum–zone waters off the Chilean coast. Science 330, 1375–1378 (2010).

    Article  Google Scholar 

  12. 12.

    Carolan, M. & Beman, J. M. Transcriptomic evidence for microbial sulfur cycling in the eastern tropical North Pacific oxygen minimum zone. Front. Microbiol. 6, 334 (2015).

    Article  Google Scholar 

  13. 13.

    Swan, B. K. et al. Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333, 1296–1300 (2011).

    Article  Google Scholar 

  14. 14.

    Alldredge, A. L. & Cohen, Y. Can microscale chemical patches persist in the sea? Microelectrode study of marine snow, fecal pellets. Science 235, 689–691 (1987).

    Article  Google Scholar 

  15. 15.

    Ploug, H. & Buchholz, B. Anoxic aggregates an ephemeral phenomenon in the ocean. Aquat. Microb. Ecol. 13, 285–294 (1997).

    Article  Google Scholar 

  16. 16.

    Klawonn, I., Bonaglia, S., Brüchert, V. & Ploug, H. Aerobic and anaerobic nitrogen transformation processes in N2-fixing cyanobacterial aggregates. ISME J. 9, 1456–1466 (2015).

    Article  Google Scholar 

  17. 17.

    Ganesh, S. et al. Size-fraction partitioning of community gene transcription and nitrogen metabolism in a marine oxygen minimum zone. ISME J. 9, 2682–2696 (2015).

    Article  Google Scholar 

  18. 18.

    Shanks, A. L. & Reeder, M. L. Reducing microzones and sulfide production in marine snow. Mar. Ecol. Prog. Ser. 96, 43–47 (1993).

    Article  Google Scholar 

  19. 19.

    Waeles, M., Maguer, J.-F., Baurand, F. & Riso, R. D. Off Congo waters (Angola Basin, Atlantic Ocean): a hot spot for cadmium-phosphate fractionation. Limnol. Oceanogr. 58, 1481–1490 (2013).

    Article  Google Scholar 

  20. 20.

    Janssen, D. J. et al. Undocumented water column sink for cadmium in open ocean oxygen-deficient zones. Proc. Natl Acad. Sci. USA 111, 6888–6893 (2014).

    Article  Google Scholar 

  21. 21.

    Simon, M., Grossart, H.-P., Schweitzer, B. & Ploug, H. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28, 175–211 (2002).

    Article  Google Scholar 

  22. 22.

    Burd, A. B. & Jackson, G. A. Particle aggregation. Annu. Rev. Mar. Sci. 1, 65–90 (2009).

    Article  Google Scholar 

  23. 23.

    Lam, P. J. & Marchal, O. Insights into particle cycling from thorium and particle data. Annu. Rev. Mar. Sci. 7, 159–184 (2015).

    Article  Google Scholar 

  24. 24.

    McDonnell, A., Boyd, P. & Buesseler, K. Effects of sinking velocities and microbial respiration rates on the attenuation of particulate carbon fluxes through the mesopelagic zone. Glob. Biogeochem. Cycles 29, 175–193 (2015).

    Article  Google Scholar 

  25. 25.

    Smayda, T. J. Normal and accelerated sinking of phytoplankton in the sea. Mar. Geol. 11, 105–122 (1971).

    Article  Google Scholar 

  26. 26.

    Jin, Q. & Bethke, C. M. Predicting the rate of microbial respiration in geochemical environments. Geochim. Cosmochim. Acta 69, 1133–1143 (2005).

    Article  Google Scholar 

  27. 27.

    Guidi, L. et al. Relationship between particle size distribution and flux in the mesopelagic zone. Deep Sea Res. Pt I 55, 1364–1374 (2008).

    Article  Google Scholar 

  28. 28.

    Durkin, C. A., Estapa, M. L. & Buesseler, K. O. Observations of carbon export by small sinking particles in the upper mesopelagic. Mar. Chem. 175, 72–81 (2015).

    Article  Google Scholar 

  29. 29.

    Ploug, H., Iversen, M. & Fischer, G. Ballast, sinking velocity and apparent diffusivity in marine snow and zooplankton fecal pellets: implications for substrate turnover by attached bacteria. Limnol. Oceanogr. 53, 1878–1886 (2008).

    Article  Google Scholar 

  30. 30.

    Picheral, M. et al. The Underwater Vision Profiler 5: an advanced instrument for high spatial resolution studies of particle size spectra and zooplankton. Limnol. Oceanogr. Methods 8, 462–473 (2010).

    Article  Google Scholar 

  31. 31.

    Weber, T., Cram, J. A., Leung, S. W., DeVries, T. & Deutsch, C. Deep ocean nutrients imply large latitudinal variation in particle transfer efficiency. Proc. Natl Acad. Sci. USA 113, 8606–8611 (2016).

    Article  Google Scholar 

  32. 32.

    Kalvelage, T. et al. Aerobic microbial respiration in oceanic oxygen minimum zones. PLoS ONE 10, e0133526 (2015).

    Article  Google Scholar 

  33. 33.

    Johnston, D. et al. Placing an upper limit on cryptic marine sulphur cycling. Nature 513, 530–533 (2014).

    Article  Google Scholar 

  34. 34.

    Martin, J. H., Knauer, G. A., Karl, D. M. & Broenkow, W. W. VERTEX: carbon cycling in the northeast Pacific. Deep Sea Res. Pt A 34, 267–285 (1987).

    Article  Google Scholar 

  35. 35.

    Ohnemus, D. C. et al. Elevated trace metal content of prokaryotic communities associated with marine oxygen deficient zones. Limnol. Oceanogr. 62, 3–25 (2017).

    Article  Google Scholar 

  36. 36.

    Lee, J.-M., Heller, M. I. & Lam, P. J. Size distribution of particulate trace elements in the US GEOTRACES Eastern Pacific Zonal Transect (GP16). Mar. Chem. (in the press).

  37. 37.

    Guidi, L. et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature 532, 465–470 (2016).

    Article  Google Scholar 

  38. 38.

    DeVries, T., Deutsch, C., Primeau, F., Chang, B. & Devol, A. Global rates of water-column denitrification derived from nitrogen gas measurements. Nat. Geosci. 5, 547–550 (2012).

    Article  Google Scholar 

  39. 39.

    Deutsch, C., Gruber, N., Key, R. M., Sarmiento, J. L. & Ganachaud, A. Denitrification and N2 fixation in the Pacific Ocean. Glob. Biogeochem. Cycles 15, 483–506 (2001).

    Article  Google Scholar 

  40. 40.

    Bianchi, D., Dunne, J. P., Sarmiento, J. L. & Galbraith, E. D. Data-based estimates of suboxia,denitrification, and N2O production in the ocean and their sensitivities to dissolved O2. Glob. Biogeochem. Cycles 26, GB2009 (2012).

    Article  Google Scholar 

  41. 41.

    Elderfield, H. & Rickaby, R. Oceanic Cd/P ratio and nutrient utilization in the glacial Southern Ocean. Nature 405, 305–310 (2000).

    Article  Google Scholar 

  42. 42.

    Franck, V. M., Bruland, K. W., Hutchins, D. A. & Brzezinski, M. A. Iron and zinc effects on silicic acid and nitrate uptake kinetics in three high-nutrient, low-chlorophyll (HNLC) regions. Mar. Ecol. Progress. Ser. 252, 15–33 (2003).

    Article  Google Scholar 

  43. 43.

    Brandes, J. A. & Devol, A. H. A global marine‐fixed nitrogen isotopic budget: implications for Holocene nitrogen cycling. Glob. Biogeochem. Cycles 16, 1120 (2002).

    Article  Google Scholar 

  44. 44.

    Deutsch, C., Sigman, D. M., Thunell, R. C., Meckler, A. N. & Haug, G. H. Isotopic constraints on glacial/interglacial changes in the oceanic nitrogen budget. Glob. Biogeochem. Cycles 18, GB4012 (2004).

    Article  Google Scholar 

  45. 45.

    DeVries, T., Deutsch, C., Rafter, P. & Primeau, F. Marine denitrification rates determined from a global 3-D inverse model. Biogeosciences 10, 2481–2496 (2013).

    Article  Google Scholar 

  46. 46.

    Großkopf, T. et al. Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature 488, 361–364 (2012).

    Article  Google Scholar 

  47. 47.

    Halm, H. et al. Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. ISME J. 6, 1238–1249 (2012).

    Article  Google Scholar 

  48. 48.

    Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).

    Article  Google Scholar 

  49. 49.

    Deutsch, C. et al. Centennial changes in North Pacific anoxia linked to tropical trade winds. Science 345, 665–668 (2014).

    Article  Google Scholar 

  50. 50.

    DeVries, T., Liang, J.-H. & Deutsch, C. A mechanistic particle flux model applied to the oceanic phosphorus cycle. Biogeosciences 11, 5381–5398 (2014).

    Article  Google Scholar 

  51. 51.

    Stemmann, L. et al. Volume distribution for particles between 3.5 to 2000 µm in the upper 200m region of the South Pacific Gyre. Biogeosciences 5, 299–310 (2008).

    Article  Google Scholar 

  52. 52.

    Jokulsdottir, T. & Archer, D. A stochastic, Lagrangian model of sinking biogenic aggregates in the ocean (SLAMS 1.0): model formulation, validation and sensitivity. Geosci. Model Dev. 9, 1455–1476 (2016).

    Article  Google Scholar 

  53. 53.

    Passow, U. & Carlson, C. A. The biological pump in a high CO2 world. Mar. Ecol. Progress. Ser. 470, 249–271 (2012).

    Article  Google Scholar 

  54. 54.

    Louca, S. et al. Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone. Proc. Natl Acad. Sci. USA 113, E5925–E5933 (2016).

    Article  Google Scholar 

  55. 55.

    Ploug, H., Hietanen, S. & Kuparinen, J. Diffusion and advection within and around sinking, porous diatom aggregates. Limnol. Oceanogr. 47, 1129–1136 (2002).

    Article  Google Scholar 

  56. 56.

    Litchman, E., Klausmeier, C. A., Schofield, O. M. & Falkowski, P. G. The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol. Lett. 10, 1170–1181 (2007).

    Article  Google Scholar 

  57. 57.

    Mullin, M., Sloan, P. & Eppley, R. Relationship between carbon content, cell volume, and area in phytoplankton. Limnol. Oceanogr. 11, 307–311 (1966).

    Article  Google Scholar 

  58. 58.

    Alldredge, A. The carbon, nitrogen and mass content of marine snow as a function of aggregate size. Deep Sea Res. Pt I 45, 529–541 (1998).

    Article  Google Scholar 

  59. 59.

    Ploug, H. & Grossart, H.-P. Bacterial growth and grazing on diatom aggregates: respiratory carbon turnover as a function of aggregate size and sinking velocity. Limnol. Oceanogr. 45, 1467–1475 (2000).

    Article  Google Scholar 

  60. 60.

    Iversen, M. H., Nowald, N., Ploug, H., Jackson, G. A. & Fischer, G. High resolution profiles of vertical particulate organic matter export off Cape Blanc, Mauritania: degradation processes and ballasting effects. Deep Sea Res. Pt I 57, 771–784 (2010).

    Article  Google Scholar 

  61. 61.

    Lee, Z. et al. Euphotic zone depth: its derivation and implication to ocean‐color remote sensing. J. Geophys. Res. Oceans 112, C03009 (2007).

    Google Scholar 

  62. 62.

    Garcia, H. et al. World Ocean Atlas 2009, Volume 3: Dissolved Oxygen, Apparent Oxygen Utilization, and Oxygen Saturation NOAA Atlas NESDIS 70 (U.S. Government Printing Office, Washington, DC, 2010).

  63. 63.

    Behrenfeld, M. J. & Falkowski, P. G. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1–20 (1997).

    Article  Google Scholar 

  64. 64.

    Carr, M.-E. et al. A comparison of global estimates of marine primary production from ocean color. Deep Sea Res. Pt II 53, 741–770 (2006).

    Article  Google Scholar 

  65. 65.

    Behrenfeld, M. J., Boss, E., Siegel, D. A. & Shea, D. M. Carbon-based ocean productivity and phytoplankton physiology from space. Glob. Biogeochem. Cycles 19, GB1006 (2005).

    Article  Google Scholar 

  66. 66.

    Dunne, J. P., Armstrong, R. A., Gnanadesikan, A. & Sarmiento, J. L. Empirical and mechanistic models for the particle export ratio. Glob. Biogeochem. Cycles 19, GB4026 (2005).

    Article  Google Scholar 

  67. 67.

    Laws, E. A., Falkowski, P. G., Smith, W. O., Ducklow, H. & McCarthy, J. J. Temperature effects on export production in the open ocean. Glob. Biogeochem. Cycles 14, 1231–1246 (2000).

    Article  Google Scholar 

  68. 68.

    Laws, E. A., D’Sa, E. & Naik, P. Simple equations to estimate ratios of new or export production to total production from satellite‐derived estimates of sea surface temperature and primary production. Limnol. Oceanogr. Methods 9, 593–601 (2011).

    Article  Google Scholar 

  69. 69.

    de Baar, H. J., Saager, P. M., Nolting, R. F. & van der Meer, J. Cadmium versus phosphate in the world ocean. Mar. Chem. 46, 261–281 (1994).

    Article  Google Scholar 

  70. 70.

    Wyatt, N. et al. Biogeochemical cycling of dissolved zinc along the GEOTRACES South Atlantic transect GA10 at 40S. Glob. Biogeochem. Cycles 28, 44–56 (2014).

    Article  Google Scholar 

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Acknowledgements

D.B. was supported by NSF grant OCE-1635632; T.S.W. was supported by NSF grant OCE-1635414; C.D. was supported by the Gordon and Betty Moore Foundation (GBMF 3775); and R.K. was supported by the German Science Foundation through the Collaborative Research Center 754 ‘Climate-Biogeochemistry Interactions in the Tropical Ocean’. We thank D. Janssen and S. John for providing trace metal data from the Mauritanian region. We further acknowledge J. Coindat and S. Fevre of Hydroptic, and L. Stemman and M. Picheral for support during work with the UVP5.

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D.B. and T.S.W. conceived the project, developed the microenvironment and particle models, conducted the simulations and analysed output, with contributions from C.D. R.K. provided UVP5 particle observations and suggested their use for model validation. D.B. and T.S.W. wrote the paper, with contributions from C.D. and R.K.

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Correspondence to Daniele Bianchi.

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Bianchi, D., Weber, T.S., Kiko, R. et al. Global niche of marine anaerobic metabolisms expanded by particle microenvironments. Nature Geosci 11, 263–268 (2018). https://doi.org/10.1038/s41561-018-0081-0

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