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Microbial control of the dark end of the biological pump

Nature Geoscience volume 6, pages 718–724 (2013)Cite this article

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Abstract

A fraction of the carbon captured by phytoplankton in the sunlit surface ocean sinks to depth as dead organic matter and faecal material. The microbial breakdown of this material in the subsurface ocean generates carbon dioxide. Collectively, this microbially mediated flux of carbon from the atmosphere to the ocean interior is termed the biological pump. In recent decades it has become clear that the composition of the phytoplankton community in the surface ocean largely determines the quantity and quality of organic matter that sinks to depth. This settling organic matter, however, is not sufficient to meet the energy demands of microbes in the dark ocean. Two additional sources of organic matter have been identified: non-sinking organic particles of debated origin that escape capture by sediment traps and exhibit stable concentrations throughout the dark ocean, and microbes that convert inorganic carbon into organic matter. Whether these two sources can together account for the significant mismatch between organic matter consumption and supply in the dark ocean remains to be seen. It is clear, however, that the microbial community of the deep ocean works in a fundamentally different way from surface water communities.

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Figure 1: The biological pump.
Figure 2: Sinking velocity of different phytoplankton size classes.
Figure 3: Processes affecting the flux of particles in the ocean.
Figure 4: Model relating the export efficiency to the transfer efficiency of the biological pump.
Figure 5: Microbial carbon demand and particulate carbon flux in the mesotrophic and oligotrophic North Atlantic.
Figure 6: Microbial inorganic carbon fixation and microbial heterotrophic production in the North Atlantic.

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References

  1. Ducklow, H. W., Steinberg, D. K. & Buesseler, K. O. Upper ocean carbon export and the biological pump. Oceanography 14, 50–58 (2001).

    Article  Google Scholar 

  2. Armstrong, R. A., Peterson, M. L., Lee, C. & Wakeham, S. G. Settling velocity sprectra and the ballast ratio hypothesis. Deep Sea Res. II 56, 1470–1478 (2009).

    Article  Google Scholar 

  3. Steinberg, D. K. et al. Bacterial vs. zooplankton control of sinking particle flux in the ocean's twilight zone. Limnol. Oceanogr. 53, 1327–1338 (2008).

    Article  Google Scholar 

  4. Reinthaler, T. et al. Prokaryotic respiration and production in the meso- and bathypelagic realm of the eastern and western North Atlantic basin. Limnol. Oceanogr. 51, 1262–1273 (2006).

    Article  Google Scholar 

  5. Alldredge, A. L. & Jackson, G. A. Aggregation in marine systems. Deep Sea Res. II 42, 1–7 (1995).

    Article  Google Scholar 

  6. Obernosterer, I. & Herndl, G. J. Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N:P ratio. Mar. Ecol. Prog. Ser. 116, 247–257 (1995).

    Article  Google Scholar 

  7. Verdugo, P. et al. The oceanic gel phase: a bridge in the DOM-POM continuum. Mar. Chem. 92, 67–85 (2004).

    Article  Google Scholar 

  8. Alldredge, A., Granata, T. C., Gotschalk, C. C. & Dickey, T. D. The physical strength of marine snow and its implications for particle dissagregation in the ocean. Limnol. Oceanogr. 35, 1415–1428 (1990).

    Article  Google Scholar 

  9. Stoderegger, K. & Herndl, G. J. Production and release of bacterial capsular material and its subsequent utilization by marine bacterioplankton. Limnol. Oceanogr. 43, 877–884 (1998).

    Article  Google Scholar 

  10. Stoderegger, K. E. & Herndl, G. J. Production of exopolymer particles by marine bacterioplankton under contrasting turbulence conditions. Mar. Ecol. Prog. Ser. 189, 9–16 (1999).

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. Kwon, E. Y., Primeau, F. & Sarmiento, J. L. The impact of remineralization depth on the air-sea carbon balance. Nature Geosci. 2, 630–635 (2009).

    Article  Google Scholar 

  13. Buesseler, K. O. & Boyd, P. W. Shedding light on processes that control particle export and flux attenuation in the twilight zone of the open ocean. Limnol. Oceanogr. 54, 1210–1232 (2009).

    Article  Google Scholar 

  14. Smetacek, V. The giant diatom dump. Nature 406, 574–575 (2000).

    Article  Google Scholar 

  15. Shatova, O., Koweek, D., Conte, M. H. & Weber, J. C. Contribution of zooplankton fecal pellets to deep ocean particle flux in the Sargasso Sea assessed using quantitative image analysis. J. Plankton Res. 34, 905–921 (2012).

    Article  Google Scholar 

  16. Richardson, T. L. & Jackson, G. A. Small phytoplankton and carbon export from the surface ocean. Science 315, 838–840 (2007).

    Article  Google Scholar 

  17. Guidi, L. et al. Effects of phytoplankton community on production, size and export of large aggregates: A world-ocean analysis. Limnol. Oceanogr. 54, 1951 (2009).

    Article  Google Scholar 

  18. Bochdansky, A. B., Aken, H. M. v. & Herndl, G. J. Role of macroscopic particles in deep-sea oxygen consumption. Proc. Natl Acad. Sci. USA 107, 8287–8291 (2010).

    Article  Google Scholar 

  19. Lampitt, R. S. & Antia, A. N. Particle flux in deep sea: regional characteristics and temporal variability. Deep Sea Res. I 44, 1377–1403 (1997).

    Article  Google Scholar 

  20. Buesseler, K. O. Do upper-ocean sediment traps provide an accurate record of particle flux? Nature 353, 420–423 (1991).

    Article  Google Scholar 

  21. Honjo, S. in Particle Flux in the Ocean. SCOPE Vol. 57 (eds Ittekot, V., Schäfer, P., Honjo, S. & Depetris, P. J.) 91–254 (Wiley, 1996).

    Google Scholar 

  22. Honjo, S. & Manganini, S. J. Annual biogenic particle fluxes to the interior of the North Atlantic Ocean; studied at 34° N 21° W and 48°N 21° W. Deep Sea Res. 40, 587–607 (1993).

    Article  Google Scholar 

  23. Buesseler, K. O. et al. A comparison of the quantity and composition of material caught in a neutrally buoyant versus surface-tethered sediment trap. Deep Sea Res. I 47, 277–294 (2000).

    Article  Google Scholar 

  24. Graham, G. W. & Smith, W. A. M. N. The application of holography to the analysis of size and settling velocity of suspended cohesive sediments. Limnol. Oceanogr. Methods 8 (1–15) (2010).

  25. Baltar, F. et al. Significance of non-sinking particulate organic carbon and dark CO2 fixation to heterotrophic carbon demand in the mesopelagic northeast Atlantic. Geophys. Res. Lett. 37, L09602 (2010).

    Article  Google Scholar 

  26. Baltar, F., Aristegui, J., Gasol, J. M., Sintes, E. & Herndl, G. J. Evidence of prokaryotic metabolism on suspended particulate organic matter in the dark waters of the subtropical North Atlantic. Limnol. Oceanogr. 54, 182–193 (2009).

    Article  Google Scholar 

  27. Dilling, L. & Allredge, A. L. Fragmentation of marine snow by swimming macrozooplankton: A new process impacting carbon cycling in the sea. Deep Sea Res. I 47, 1227–1245 (2000).

    Article  Google Scholar 

  28. Alonso-González, I. J. et al. Role of slowly settling particles in the ocean carbon cycle. Geophys. Res. Lett. 37, L13608 (2010).

    Article  Google Scholar 

  29. Goutx, M. et al. Composition and degradation of marine particles with different settling velocities in the northwestern Mediterranean Sea. Limnol. Oceanogr. 52, 1645–1664 (2007).

    Article  Google Scholar 

  30. Abramson, L., Lee, C., Liu, Z., Wakeham, S. G. & Szlosek, J. Exchange between suspended and sinking particles in the northwest Mediterranean as inferred from the organic composition of in situ pump and sediment trap samples. Limnol. Oceanogr. 55, 725–739 (2010).

    Article  Google Scholar 

  31. Druffel, E. R. M., Bauer, J. E., Griffin, S. & Hwang, J. Penetration of anthropogenic carbon into organic particles of the deep ocean. Geophys. Res. Lett. 30 (2003).

  32. Riley, J. S. et al. The relative contribution of fast and slow sinking particles to ocean carbon export. Global Biogeochem. Cycles 26 (2012).

    Article  Google Scholar 

  33. Karl, D. M., Knauer, G. A. & Martin, J. H. Downward flux of particulate organic matter in the ocean: a particle decomposition paradox. Nature 332, 438–441 (1988).

    Article  Google Scholar 

  34. Cho, B. C. & Azam, F. Major role of bacteria in biogeochemical fluxes in the ocean's interior. Nature 332, 441–443 (1988).

    Article  Google Scholar 

  35. Kellogg, C. T. E. et al. Evidence for microbial attenuation of particle flux in the Amundsen Gulf and Beaufort Sea: elevated hydrolytic enzyme activity on sinking aggregates. Polar Biol. 34, 2007–2023 (2011).

    Article  Google Scholar 

  36. Grossart, H.-P. & Gust, G. Hydrostatic pressure affects physiology and community structure of marine bacteria during settling to 4000 m: an experimental approach. Mar. Ecol. Prog. Ser. 390, 97–104 (2009).

    Article  Google Scholar 

  37. Tamburini, C. et al. Pressure effects on surface Mediterranean prokaryotes and biogenic silica dissolution during a diatom sinking experiments. Aquat. Microb. Ecol. 43, 267–276 (2006).

    Article  Google Scholar 

  38. Hansell, D. A., Carlson, C. A. & Schlitzer, R. Net removal of major marine dissolved organic carbon fractions in the subsurface ocean. Glob. Biogeochem. Cycles 26, GB1016 (2012).

    Article  Google Scholar 

  39. Druffel, E. R. M. & Robison, B. H. Is the deep sea on a diet? Science 284, 1139–1140 (1999).

    Article  Google Scholar 

  40. Druffel, E. R. M. & Williams, P. M. Identification of a deep marine source of particulate organic carbon using bomb 14C. Nature 347, 172–174 (1990).

    Article  Google Scholar 

  41. Lauro, F. M. et al. The genomic basis of trophic strategy in marine bacteria. Proc. Natl Acad. Sci. USA 106, 15527–15533 (2009).

    Article  Google Scholar 

  42. Moeseneder, M. M., Winter, C. & Herndl, G. J. Horizontal and vertical complexity of attached and free-living bacteria of the eastern Mediterranean Sea, determined by 16S rDNA and 16S rRNA fingerprints. Limnol. Oceanogr. 46, 95–107 (2001).

    Article  Google Scholar 

  43. Aristegui, J., Gasol, J. M., Duarte, C. M. & Herndl, G. J., Microbial oceanography of the dark ocean's pelagic realm. Limnol. Oceanogr. 54, 1501–1529 (2009).

    Article  Google Scholar 

  44. Eloe, E. A. et al., Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep-ocean environment. Environ. Microbiol. Rep. 3, 449–458 (2011).

    Article  Google Scholar 

  45. Lauro, F. M. & Bartlett, D. H., Prokaryotic lifestyles in deep sea habitats. Extremophiles 12, 15–25 (2007).

    Article  Google Scholar 

  46. Lauro, F. M., Chastain, R. A., Blankenship, L. E., Yayanos, A. A. & Bartlett, D. H. The unique 16S rRNA genes of piezophiles reflect both phylogeny and adaptation. Appl. Environ. Microbiol. 73, 838–845 (2007).

    Article  Google Scholar 

  47. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311, 496–503 (2006).

    Article  Google Scholar 

  48. Martin-Cuadrado, A-B. et al. Metagenomics of deep Mediterranean, a warm bathypelagic habitat. PLoS One 9, e914 (2007).

    Article  Google Scholar 

  49. Ivars-Martinez, E. et al. Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J. 2, 1194–1212 (2008).

    Article  Google Scholar 

  50. Vetter, Y. A., Deming, J. W., Jumars, P. A. & Krieger-Brockett, B. B. A predicitive model of bacterial foraging by means of freely released extracellular enzymes. Microb. Ecol. 36, 75–92 (1998).

    Article  Google Scholar 

  51. Baltar, F. et al. High dissolved extracellular enzymatic activity in the deep central Atlantic Ocean. Aquat. Microb. Ecol. 58, 287–302 (2010).

    Article  Google Scholar 

  52. Antia, A. N. et al. Basin-wide particulate carbon flux in the Atlantic Ocean: regional export patterns and potential for athmospheric CO2 sequestration. Glob. Biogeochem. Cycles 15, 845–862 (2001).

    Article  Google Scholar 

  53. Yokokawa, T., Yang, Y., Motegi, C. & Nagata, T. Large-scale geographical variation in prokaryotic abundance and production in meso- and bathypelagic zones of the central Pacific and Southern Ocean. Limnol. Oceanogr. 58, 61–73 (2013).

    Article  Google Scholar 

  54. Aristegui, J. et al. Dissolved organic carbon support of respiration in the dark ocean. Science 298, 1967 (2002).

    Article  Google Scholar 

  55. Alonso-Saez, L., Galand, P. E., Casamayor, E. O., Pedros-Alio, C. & Bertilsson, S. High bicarbonate assimilation in the dark by Arctic bacteria. ISME J. 4, 1581–1590 (2010).

    Article  Google Scholar 

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

    Article  Google Scholar 

  57. Anantharaman, K., Breier, J. A., Sheik, C. S. & Dick, G. J. Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc. Natl Acad. Sci. USA 110, 330–335 (2013).

    Article  Google Scholar 

  58. Hügler, M. & Sievert, S. M. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annu. Rev. Mar. Sci. 3, 261–289 (2011).

    Article  Google Scholar 

  59. Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nature Rev. Microbiol. 5, 782–791 (2007).

    Article  Google Scholar 

  60. Reinthaler, T., Aken, H. M.v. & Herndl, G. J. Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic's interior. Deep Sea Res. II 57, 1572–1580 (2010).

    Article  Google Scholar 

  61. Yakimov, M. M. et al., Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea). ISME J. 5, 945–961 (2011).

    Article  Google Scholar 

  62. Burd, A. B. et al. Assessing the apparent imbalance between geochemcial and biochemical indicators of meso- and bathypelagic biological activity: What the @$#! is wrong with present calculations of carbon budgets. Deep Sea Res. II 57, 1557–1571 (2010).

    Article  Google Scholar 

  63. Jiao, N. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Rev. Microbiol. 8, 593–599 (2010).

    Article  Google Scholar 

  64. Bauer, J. E., Williams, P. M. & Druffel, E. R. M. 14C activity of dissolved organic carbon fractions in the north-central Pacific and Sargasso Sea. Nature 357, 667–670 (1992).

    Article  Google Scholar 

  65. Carlson, C. A. et al. Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea. Limnol. Oceanogr. 49, 1073–1083 (2004).

    Article  Google Scholar 

  66. Shi, Y., McCarren, J. & Delong, E. F. Transcriptional responses of surface water marine microbial assemblages to deep-sea water amendment. Environ. Microbiol. 14, 191–206 (2012).

    Article  Google Scholar 

  67. Nagata, T. et al. Emerging concepts on microbial processes int he bathypelagic ocean: ecology, biogeochemistry and genomics. Deep Sea Res. II 57, 1519–1536 (2010).

    Article  Google Scholar 

  68. Tamburini, C., Boutrif, M., Garel, M., Colwell, R. R. & Deming, J. W. Prokaryotic responses to hydrostatic pressure in the ocean: a review. Environ. Microbiol. (2013).

  69. Riebesell, U., Körtzinger, A. & Oschlies, A. Sensitivities of marine carbon fluxes to ocean change. Proc. Natl Acad. Sci. USA 106, 20602–20609 (2009).

    Article  Google Scholar 

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Acknowledgements

This work was supported by the ERC Advanced Grant MEDEA and the Austrian Science Fund projects: I486-B09 and P23234-B11 to G.J.H. and P23221-B11 to T.R.

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Authors and Affiliations

  1. Department of Limnology and Oceanography, University of Vienna, Althanstrasse 14, Vienna, A-1090, Austria

    Gerhard J. Herndl & Thomas Reinthaler

  2. Department of Biological Oceanography, Royal Netherlands Institute for Sea Research, Texel, 1790 AB Den Burg, The Netherlands

    Gerhard J. Herndl

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G.J.H. and T.R. contributed equally to this work.

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Correspondence to Gerhard J. Herndl.

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Herndl, G., Reinthaler, T. Microbial control of the dark end of the biological pump. Nature Geosci 6, 718–724 (2013). https://doi.org/10.1038/ngeo1921

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