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Microbial oceanography: paradigms, processes and promise

Key Points

  • Microorganisms are the dominant organisms in the sea, both in terms of mass and ecological importance.

  • Most marine microorganisms have not yet been brought into pure cultures in the laboratory, so detailed information about their ecological roles is incomplete.

  • New molecular tools, including gene-based approaches, are beginning to provide data on the diversity and metabolic processes of novel microorganisms that are not yet in culture.

  • The new discipline of microbial oceanography endeavours to observe and understand microbial life in the sea well enough to make accurate ecological predictions of, for example, the impact of climate variations on microbial processes in the sea.

  • Research in microbial oceanography requires an interdisciplinary approach that includes: understanding the physical and chemical habitat properties; making observations over a broad range of time and space scales; designing and implementing hypothesis-testing field experiments; and integrating data into ecosystem-based models. These interdisciplinary interactions must be between scientists who have not traditionally worked together.

  • We are at a unique point in time — one that is characterized by important challenges and great opportunities. New training programmes to prepare the next generation of microbial oceanographers will be essential for continued progress in this important discipline.

Abstract

Life on Earth most likely originated as microorganisms in the sea. Over the past 3.5 billion years, microorganisms have shaped and defined Earth's biosphere and have created conditions that have allowed the evolution of macroorganisms and complex biological communities, including human societies. Recent advances in technology have highlighted the vast and previously unknown genetic information that is contained in extant marine microorganisms, from new protein families to novel metabolic processes. Now there is a unique opportunity, using recent advances in molecular ecology, metagenomics, remote sensing of microorganisms and ecological modelling, to achieve a comprehensive understanding of marine microorganisms and their susceptibility to environmental variability and climate change. Contemporary microbial oceanography is truly a sea of opportunity and excitement.

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Figure 1: Solar energy flux and capture in the sea.
Figure 2: Oxygen concentrations and dynamics at the HOT Station ALOHA (22.75°N, 158°W).
Figure 3: Effects of nutrient perturbations on open-ocean ecosystems.
Figure 4: The relationships between inorganic phosphorus and dissolved organic phosphorus.

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Tara Ocean Foundation, Tara Oceans, … European Marine Biological Resource Centre - European Research Infrastructure Consortium (EMBRC-ERIC)

References

  1. Karl, D. M. & Proctor, L. Foundations of microbial oceanography. Oceanography 20, 14–25 (2007).

    Article  Google Scholar 

  2. Duarte, C. M., Gasol, J. M. & Vaque, D. Role of experimental approaches in marine microbial ecology. Aquat. Microb. Ecol. 13, 101–111 (1997).

    Article  Google Scholar 

  3. Doney, S. C., Abbott, M. R., Cullen, J. J., Karl, D. M. & Rothstein, L. From genes to ecosystems: the ocean's new frontier. Frontiers Ecol. Environ. 2, 457–466 (2004). This majestic review is one of the first to establish the importance of environmental genomics as an integral component of marine-ecosystem research.

    Article  Google Scholar 

  4. Rothstein, L. M. et al. Modeling ocean ecosystems: The PARADIGM program. Oceanography 19, 17–45 (2006).

    Article  Google Scholar 

  5. van Leeuwenhoek, A. Concerning little animals by him observed in rain-, well-, sea- and snow-water; as also in water wherein pepper had lain infused. Phil. Trans. Royal Soc. London 12, 821–831 (1677).

    Article  Google Scholar 

  6. Karl, D. M. & Dore, J. E. in Methods in Microbiology Vol. 30 (ed. Paul, J. H.), 13–39 (Academic Press, San Diego, 2001).

    Google Scholar 

  7. Rusch, D. B. et al. The Sorcerer II global ocean sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5, 0398–0431 (2007). This paper, one of a collection of articles from the recently completed global ocean sampling expedition (see also reference 14), presents an extensive metagenomic data set (6billion base pairs) for surface-water marine microorganisms.

    Article  CAS  Google Scholar 

  8. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hunter-Cevera, J., Karl, D. & Buckley, M. Marine Microbial Diversity: The Key to Earth's Habitability (American Academy of Microbiology, Washington, DC, 2005).

    Google Scholar 

  10. Pace, N. R. A molecular view of microbial diversity and the biosphere. Science 276, 734–740 (1997).

    Article  CAS  PubMed  Google Scholar 

  11. Sogin, M. L. et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc. Natl Acad. Sci. USA 103, 12115–12120 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tringe, S. G. & Rubin, E. M. Metagenomics: DNA sequencing of environmental samples. Nature Rev. Genetics 6, 805–814 (2005).

    Article  CAS  Google Scholar 

  13. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Yooseph, S. et al. The Sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biol. 5, 0432–0466 (2007).

    Article  CAS  Google Scholar 

  15. Ryther, J. H. Potential productivity of the sea. Science 130, 602–608 (1959).

    Article  CAS  PubMed  Google Scholar 

  16. Kolber, Z. Energy cycle in the ocean: powering the microbial world. Oceanography 20, 82–91 (2007).

    Article  Google Scholar 

  17. Cullen, J. J., Franks, P. J. S., Karl, D. M. & Longhurst, A. in The Sea Vol. 12 (eds Robinson, A. R., McCarthy, J. J. & Rothschild, B. J.) 297–336 (John Wiley & Sons, Inc., New York, 2002). A comprehensive review that combines theory, observations and models for the role of physical forcing on the structure and dynamics of marine ecosystems, including microbial biogeochemical processes.

    Google Scholar 

  18. Béjà, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000). This paper is the first report of proteorhodopsin in the sea, a novel protein that functions as a light-driven proton pump.

    Article  PubMed  Google Scholar 

  19. Martinez, A., Bradley, A. S., Waldbauer, J. R., Summons, R. E. & DeLong, E. F. Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. Proc. Natl Acad. Sci. USA 104, 5590–5595 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Karl, D. M. Hidden in a sea of microbes. Nature 415, 590–591 (2002).

    Article  CAS  PubMed  Google Scholar 

  21. Giovannoni, S. J. et al. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85 (2005).

    Article  CAS  PubMed  Google Scholar 

  22. Gómez-Consarnau, L. et al. Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445, 210–213 (2007). This is the first report of proteorhodopsin-based energy capture in a cultivated marine microorganism that shows enhanced cell yield when grown in the light.

    Article  CAS  PubMed  Google Scholar 

  23. del Giorgio, P. A., Cole, J. J. & Cimbleris, A. Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385, 148–151 (1997).

    Article  CAS  Google Scholar 

  24. Duarte, C. M. & Agusti, S. The CO2 balance of unproductive aquatic ecosystems. Science 281, 234–236 (1998).

    Article  CAS  PubMed  Google Scholar 

  25. Williams, P. J. le B., Morris, P. J. & Karl, D. M. Net community production and metabolic balance at the oligotrophic ocean site, Station ALOHA. Deep-Sea Res. I 51, 1563–1578 (2004).

    Article  CAS  Google Scholar 

  26. Karl, D. M., Laws, E. A., Morris, P., Williams, P. J. leB. & Emerson, S. Metabolic balance of the open sea. Nature 426, 32 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. Platt, T. et al. Biological production of the oceans: the case for a consensus. Mar. Ecol. Prog. Ser. 52, 77–88 (1989).

    Article  Google Scholar 

  28. McGowan, J. A. & Hayward, T. L. Mixing and oceanic productivity. Deep-Sea Res. 25, 771–793 (1978).

    Article  Google Scholar 

  29. McGillicuddy, D. J. Jr et al. Influence of mesoscale eddies on new production in the Sargasso Sea. Nature 394, 263–266 (1998).

    Article  CAS  Google Scholar 

  30. Uz, B. M., Yoder, J. A. & Osychny, V. Pumping of nutrients to ocean surface waters by the action of propagating planetary waves. Nature 409, 597–600 (2001).

    Article  CAS  PubMed  Google Scholar 

  31. McAndrew, P. M. et al. Metabolic response of oligotrophic plankton communities to deep water nutrient enrichment. Mar. Ecol. Prog. Ser. 332, 63–75 (2007).

    Article  CAS  Google Scholar 

  32. Dachs, J. et al. High atmosphere-ocean exchange of organic carbon in the NE subtropical Atlantic. Geophys. Res. Lett. 32, L21807 (2005).

    Article  CAS  Google Scholar 

  33. DeLong, E. F. Archaea in coastal marine environments. Proc. Natl Acad. Sci. USA 89, 5685–5689 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Fuhrman, J. A., McCallum, K. & Davis, A. A. Novel major archaebacterial group from marine plankton. Nature 356, 148–149 (1992).

    Article  CAS  PubMed  Google Scholar 

  35. DeLong, E. F., Wu, K. Y., Prezelin, B. B. & Jovine, R. V. High abundance of Archaea in Antarctic marine picoplankton. Nature 371, 695–697 (1994).

    Article  CAS  PubMed  Google Scholar 

  36. Massana, R., Murray, A. E., Preston, C. M. & DeLong, E. F. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara channel. Appl. Environ. Microbiol. 63, 50–56 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. DeLong, E. F. Microbial domains in the ocean: a lesson from the Archaea. Oceanography 20, 124–129 (2007).

    Article  Google Scholar 

  39. Karl, D. M., Knauer, G., Martin, J. & Ward, B. Bacterial chemolithotrophy in the ocean is associated with sinking particles. Nature 309, 54–56 (1984).

    Article  CAS  Google Scholar 

  40. Pearson, A., McNichol, A. P., Benitez-Nelson, C., Hayes, J. M. & Eglinton, T. I. Origins of lipid biomarkers in Santa Monica Basin surface sediment: a case study using compound-specific 14C analysis. Geochim. Cosmochim. Acta 65, 3123–3137 (2001).

    Article  CAS  Google Scholar 

  41. Wuchter, C., Schouten, S., Boschker, H. T. & Sinninghe Damste, J. S. Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol. Lett. 219, 203–207 (2003).

    Article  CAS  PubMed  Google Scholar 

  42. Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005). The first paper to report the isolation and cultivation of an ammonia-oxidizing marine archaeon.

    Article  CAS  PubMed  Google Scholar 

  43. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Nicol, G. W. & Schleper, C. Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? Trends Microbiol. 14, 207–212 (2006).

    Article  CAS  PubMed  Google Scholar 

  45. Wuchter, C. et al. Archaeal nitrification in the ocean. Proc. Natl Acad. Sci. USA 103, 12317–12322 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Schleper C., Jurgens, G. & Jonuscheit, M. Genomic studies of uncultivated archaea. Nature Rev. Microbiol. 3, 479–488 (2005).

    Article  CAS  Google Scholar 

  47. Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E. & Oakley, B. B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl Acad. Sci. USA 102, 14683–14688 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Mincer, T. J. et al. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 1162–1175 (2007).

    Article  CAS  PubMed  Google Scholar 

  49. Costa, E., Pérez, J. & Kreft, J.-U. Why is metabolic labour divided in nitrification? Trends Microbiol. 14, 213–219 (2006).

    Article  CAS  PubMed  Google Scholar 

  50. Ouverney, C. C. & Fuhrman, J. A. Marine planktonic Archaea take up amino acids. Appl. Environ. Microbiol. 66, 4829–4833 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Herndl, G. J. et al. Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl. Environ. Microbiol. 71, 2303–2309 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Teira, E., van Aken, H., Veth, C. & Herndl, G. J. Archaeal uptake of enantiomeric amino acids in the meso- and bathypelagic waters of the North Atlantic. Limnol. Oceanogr. 51, 60–69 (2006).

    Article  CAS  Google Scholar 

  53. Hallam, S. J. et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4, 0520–0536 (2006).

    Article  CAS  Google Scholar 

  54. Karl, D. M. A sea of change: biogeochemical variability in the North Pacific Subtropical Gyre. Ecosystems 2, 181–214 (1999).

    Article  CAS  Google Scholar 

  55. Michaels, A. F., Karl, D. M. & Capone, D. G. Element stoichiometry, new production and nitrogen fixation. Oceanography 14, 68–77 (2001).

    Article  Google Scholar 

  56. Karl, D. M. et al. in Nitrogen in the Marine Environment (eds Bronk, D., Mulholland, M., Capone, D. & Carpenter, E.) in press (Academic Press).

  57. Karl, D. et al. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538 (1997).

    Article  CAS  Google Scholar 

  58. Dore, J. E., Brum, J. R., Tupas, L. M. & Karl, D. M. Seasonal and interannual variability in sources of nitrogen supporting export in the oligotrophic subtropical North Pacific Ocean. Limnol. Oceanogr. 47, 1595–1607 (2002).

    Article  CAS  Google Scholar 

  59. Bertilsson, S., Berglund, O., Karl, D. M. & Chisholm, S. W. Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48, 1721–1731 (2003).

    Article  CAS  Google Scholar 

  60. White, A., Spitz, Y., Karl, D. M. & Letelier, R. M. Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications. Limnol. Oceanogr. 51, 1777–1790 (2006).

    Article  CAS  Google Scholar 

  61. Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton University Press, Princeton, 2002).

    Google Scholar 

  62. Karl, D. M. in Manual of Environmental Microbiology, Third Edition (eds Hurst, C. J. et al.) (American Society of Microbiology Press, Washington D. C., 2007).

    Google Scholar 

  63. Karl, D. M. Nutrient dynamics in the deep blue sea. Trends Microbiol. 10, 410–418 (2002).

    Article  CAS  PubMed  Google Scholar 

  64. Schindler, D. W. Replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1, 323–334 (1998).

    Article  Google Scholar 

  65. de Baar, H. J. W. et al. Synthesis of iron fertilization experiments: from the Iron Age to the Age of Enlightenment. J. Geophys. Res. 110, C09S16 (2005).

    Article  CAS  Google Scholar 

  66. Boyd, P. W. et al. Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315, 612–617 (2007). A comprehensive summary and ecological synthesis of the design and implementation of deliberate iron-fertilization experiments in the open sea.

    Article  CAS  PubMed  Google Scholar 

  67. Thingstad, T. F. et al. Nature of phosphorus limitation in the ultraoligotrophic Eastern Mediterranean. Science 309, 1068–1071 (2005).

    Article  CAS  PubMed  Google Scholar 

  68. Berman, T., Walline, P. D., Schneller, A., Rothenberg, J. & Townsend, D. W. Secchi disk depth record: a claim for the Eastern Mediterranean. Limnol. Oceanogr. 30, 447–448 (1985).

    Article  Google Scholar 

  69. Krom, M. D., Kress, N., Brenner, S. & Gordon, L. I. Phosphorus limitation of primary productivity in the Eastern Mediterranean Sea. Limnol. Oceanogr. 36, 424–432 (1991).

    Article  CAS  Google Scholar 

  70. Rees, A. P., Law, C. S. & Woodward, E. M. S. High rates of nitrogen fixation during an in-situ phosphate release experiment in the Eastern Mediterranean Sea. Geophys. Res. Lett. 33, L10607 (2006).

    Article  CAS  Google Scholar 

  71. Krom, M. D. Preface: CYCLOPS dedicated volume. Deep-Sea Res. II 52, 2877–2878 (2005).

    Article  Google Scholar 

  72. Chisholm, S. W., Falkowski, P. G. & Cullen, J. J. Dis-crediting ocean fertilization. Science 294, 309–310 (2001).

    Article  CAS  PubMed  Google Scholar 

  73. Doney, S. C. The dangers of ocean acidification. Sci. Amer. 294, 58–65 (2006).

    Article  PubMed  Google Scholar 

  74. ZoBell, C. E. Marine Microbiology: a Monograph on Hydrobacteriology (Chronica Botanica Company, Waltham, 1946).

    Google Scholar 

  75. Wood, E. J. F. Marine Microbial Ecology (Reinhold Publishing Corp., New York, 1965).

    Google Scholar 

  76. Sieburth, J. McN., Smetacek, V. & Lenz, J. Pelagic ecosystem structure: heterotrophic compartments of plankton and their relationship to plankton size fractions. Limnol. Oceanogr. 23, 1256–1263 (1978).

    Article  Google Scholar 

  77. Waterbury, J. B., Watson, S. W., Guillard, R. R. L. & Brand, L. E. Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature, 277, 293–294 (1979).

    Article  Google Scholar 

  78. Chisholm, S. W., Olson, R. J., Zettler, E. R., Goericke, R., Waterbury, J. B. & Welschmeyer, N. A. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334, 340–343 (1988). This paper was the first report of Prochlorococcus in the sea; this and subsequent work have established this microorganism as one of the most important photolithoautotrophs on Earth.

    Article  Google Scholar 

  79. Pace, N. R. Time for a change. Nature 441, 289 (2006).

    Article  CAS  PubMed  Google Scholar 

  80. Longhurst, A. Ecological Geography of the Sea (Academic Press, San Diego, 1998).

    Google Scholar 

  81. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311, 496–503 (2006). A pioneering study that describes genomic variability at Station ALOHA along the depth continuum from the well-lit surface waters to the deep abyss.

    Article  CAS  PubMed  Google Scholar 

  82. Karl, D. M. & Lukas, R. The Hawaii ocean time-series (HOT) program: background, rationale and field implementation. Deep-Sea Res. II 43, 129–156 (1996).

    Article  CAS  Google Scholar 

  83. Karl, D. M., Bidigare, R. R. & Letelier, R. M. Long-term changes in plankton community structure and productivity in the North Pacific Subtropical Gyre: the domain shift hypothesis. Deep-Sea Res. II 48, 1449–1470 (2001).

    Article  Google Scholar 

  84. Corno, G. et al. Impact of climate forcing on ecosystem processes in the North Pacific Subtropical Gyre. J. Geophys. Res. 112, C04021 (2007).

    Article  Google Scholar 

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Acknowledgements

I thank the HOT and C-MORE program scientists and staff for their important contributions, and the National Science Foundation, the Agouron Institute and the Gordon and Betty Moore Foundation for generous financial support of my research and training endeavors.

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DATABASES

Entrez Genome Project

Cenarchaeum symbiosum

Escherichia coli

Nitrosopumilus maritimus

Candidatus Pelagibacter ubique

Prochlorococcus

Synechococcus

FURTHER INFORMATION

David Karl's homepage

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C-MORE

Laboratory for Microbial Oceanography

Glossary

Phototrophic

Able to fix inorganic carbon using energy from light.

Heterotrophic

Able to acquire metabolic energy by the consumption of particulate or dissolved organic matter.

Microheterotrophs

Small (2–20 m) prokaryotic or eukaryotic organisms that are dependent on organic matter.

Bacterioplankton

Bacteria that inhabit the water column of lakes and oceans, either freely suspended or attached to particles.

Oligotrophic

Having low levels of nutrient and algal photosynthetic production (for example, the open ocean).

Radiative forcing

The difference between the incoming radiation energy and the outgoing radiation energy in a given climate system.

Terrigenous

Derived from land or terrestrial ecosystems.

Pelagic

Water-column portion of marine and fresh-water habitats.

Euphotic zone

Upper realms of the oceans (or lakes) that are penetrated by sufficient amounts of light for photosynthetic organisms to grow.

Primary production

Process during which carbon dioxide is incorporated into organic matter by bacteria and algae, using any of a variety of energy sources.

Mixotrophs

Organisms that are part autotrophic and part heterotrophic, such as carnivorous plants.

Autotrophy

The acquisition of metabolic energy from the fixation of inorganic carbon, for example, by photo- or chemosynthesis.

Picoplankton

Organisms that are suspended in the water column that are less than 2 mm in size.

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Karl, D. Microbial oceanography: paradigms, processes and promise. Nat Rev Microbiol 5, 759–769 (2007). https://doi.org/10.1038/nrmicro1749

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