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Microbial oceanography and the Hawaii Ocean Time-series programme

Nature Reviews Microbiology volume 12, pages 699–713 (2014)Cite this article

Subjects

Key Points

  • Marine habitats and the ecosystems that they support are diverse, complex and grossly undersampled, despite their importance to global processes and planetary habitability.

  • Microbially mediated biogeochemical cycles and metabolism are time-variable, climate-sensitive, non-steady-state processes and must be studied as such.

  • Microbial community structure, gene regulation and population interactions are dynamic features of marine ecosystems with substantial variation on multiple time scales, ranging from diel to decadal, and beyond.

  • Long-term (>1 decade), time series observations of microbial and biogeochemical processes provide invaluable data on genetic diversity and evolution, as well as the environmental controls on fundamental fluxes of energy and matter.

  • The establishment of long-term microbial observatories, including programmes like the Hawaii Ocean Time-series (HOT) provide platforms for collaborative research, support the conduct of transdisciplinary hypothesis-testing field experiments, and function as loci for the education and training of the next generation of leaders.

  • The relatively new discipline of microbial oceanography represents enormous opportunity to develop a more comprehensive understanding of the impacts of humans on microbial processes in the sea.

Abstract

The Hawaii Ocean Time-series (HOT) programme has been tracking microbial and biogeochemical processes in the North Pacific Subtropical Gyre since October 1988. The near-monthly time series observations have revealed previously undocumented phenomena within a temporally dynamic ecosystem that is vulnerable to climate change. Novel microorganisms, genes and unexpected metabolic pathways have been discovered and are being integrated into our evolving ecological paradigms. Continued research, including higher-frequency observations and at-sea experimentation, will help to provide a comprehensive scientific understanding of microbial processes in the largest biome on Earth.

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Figure 1: Station ALOHA habitat characteristics.
Figure 2: Selected examples of temporal variability in the NPSG.
Figure 3: Prochlorococcus spp. distributions and dynamics.
Figure 4: Temporal and depth variability in primary production at Station ALOHA.

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Article 30 June 2022

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

References

  1. Hooke, R. Micrographia: Some Physiological Descriptions of Minute Bodies made by Magnifying Glasses. With Observations and Inquiries Thereupon. (J. Martyn & J. Allestry, 1665).

    Google Scholar 

  2. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    CAS  PubMed  Google Scholar 

  3. Karl, D. M. & Schlesinger, W. H. (eds) Treatise on Geochemistry Vol. 10 (Elsevier, 2013).

    Google Scholar 

  4. Sverdrup, H. U., Johnson, M. W. & Fleming, R. H. The Oceans: Their Physics, Chemistry and General Biology (Prentice-Hall, 1946).

    Google Scholar 

  5. Blackburn, M. in Analysis of Marine Ecosystems (ed. Longhurst, A. R.), 3–29 (Academic Press, 1981).

    Google Scholar 

  6. McGowan, J. A. & Walker, P. W. Dominance and diversity maintenance in an oceanic ecosystem. Ecol. Monogr. 55, 103–118 (1985).

    Google Scholar 

  7. Clements, F. E. Nature and structure of the climax. J. Ecol. 24, 253–284 (1936).

    Google Scholar 

  8. 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).

    Google Scholar 

  9. Johnson, P. W. & Sieburth, J. McN. Chroococcoid cyanobacteria in the sea: a ubiquitous and diverse phototrophic biomass. Limnol. Oceanogr. 24, 928–935 (1979).

    Google Scholar 

  10. Azam, F. et al. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263 (1983).

    Google Scholar 

  11. Breitbart, M. Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4, 425–448 (2012).

    Google Scholar 

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

    CAS  Google Scholar 

  13. Karl, D. M. A sea of change: biogeochemical variability in the North Pacific subtropical gyre. Ecosystems 2, 181–214 (1999). This paper uses the synthesis of HOT programme observations to highlight the scales of variability in the subtropical North Pacific Ocean and describes the role of microorganism metabolism in maintaining the habitability of this ecosystem.

    CAS  Google Scholar 

  14. Karl, D. M. et al. in Ocean Biogeochemistry: The Role of the Ocean Carbon Cycle in Global Change (ed. Fasham, M. J. R.) 239–267 (Springer, 2003).

    Google Scholar 

  15. Church, M. J., Lomas, M. W. & Muller-Karger, F. Sea change: charting the course for biogeochemical ocean time series research in a new millennium. Deep Sea Res. Part II 93, 2–15 (2013).

    CAS  Google Scholar 

  16. Eppley, R. W. The PRPOOS program: a study of plankton rate processes in oligotrophic oceans. Eos 63, 522–523 (1982).

    Google Scholar 

  17. Williams, P. J. le B., Heinemann, K. R., Marra, J. & Purdie, D. A. Comparison of 14C and O2 measurements of phytoplankton production in oligotrophic waters. Nature 305, 49–50 (1983).

    CAS  Google Scholar 

  18. Laws, E. A. et al. High phytoplankton growth and production rates in oligotrophic Hawaiian coastal waters. Limnol. Oceanogr. 29, 1161–1169 (1984).

    CAS  Google Scholar 

  19. Hayward, T. L. Primary production in the North Pacific Central Gyre: a controversy with important implications. Trends Ecol. Evol. 6, 281–284 (1991).

    CAS  PubMed  Google Scholar 

  20. Eppley, R. W., Renger, E. H., Venrick, E. L. & Mullin, M. M. A study of plankton dynamics and nutrient cycling in the central gyre of the North Pacific Ocean. Limnol. Oceanogr. 18, 534–551 (1973).

    CAS  Google Scholar 

  21. Gundersen, K. R. et al. Structure and biological dynamics of the oligotrophic ocean photic zone off the Hawaiian islands. Pac. Sci. 30, 45–68 (1976).

    CAS  Google Scholar 

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

    Google Scholar 

  23. Venrick, E. L. Phytoplankton in an oligotrophic ocean: observations and questions. Ecol. Monogr. 52, 129–154 (1982).

    Google Scholar 

  24. Venrick, E. L., McGowan, J. A., Cayan, D. R. & Hayward, T. L. Climate and chlorophyll a: long-term trends in the central North Pacific Ocean. Science 238, 70–72 (1987). This paper provides one of the first assessments of the closely coupled nature of climate variability and plankton dynamics in the subtropical North Pacific.

    CAS  PubMed  Google Scholar 

  25. Fong, A. A. et al. Nitrogen fixation in an anticyclonic eddy in the oligotrophic North Pacific Ocean. ISME J. 2, 663–676 (2008).

    CAS  PubMed  Google Scholar 

  26. Dore, J. E., Letelier, R. M., Church, M. J., Lukas, R. & Karl, D. M. Summer phytoplankton blooms in the oligotrophic North Pacific Subtropical Gyre: historical perspective and recent observations. Prog. Oceanogr. 76, 2–38 (2008).

    Google Scholar 

  27. Villareal, T. A., Brown, C. G., Brzezinski, M. A., Krause, J. W. & Wilson, C. Summer diatom blooms in the North Pacific subtropical gyre: 2008–2009. PLoS ONE 7, e33109 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Letelier, R. M. et al. Role of late winter mesoscale events in the biogeochemical variability of the upper water column of the North Pacific Subtropical Gyre. J. Geophys. Res. 105, 28723–28739 (2000).

    CAS  Google Scholar 

  29. Sakamoto, C. M. et al. Influence of Rossby waves on nutrient dynamics and the plankton community structure in the North Pacific subtropical gyre. J. Geophys. Res. 109, C05032 (2004).

    Google Scholar 

  30. White, A. E., Spitz, Y. H. & Letelier, R. M. What factors are driving summer phytoplankton blooms in the North Pacific Subtropical Gyre? J. Geophys. Res. 112, C12006 (2007).

    Google Scholar 

  31. Guidi, L. et al. Does eddy–eddy interaction control surface phytoplankton distribution and carbon export in the North Pacific Subtropical Gyre? J. Geophys. Res. 117, G02024 (2012).

    Google Scholar 

  32. Lukas, R. & Santiago-Mandujano, F. Extreme water mass anomaly observed in the Hawaii Ocean Time Series. Geophys. Res. Lett. 28, 2931–2934 (2001).

    CAS  Google Scholar 

  33. Keeling, C. D. et al. Atmospheric carbon dioxide variations at Mauna Loa Observatory, Hawaii. Tellus 28, 538–551 (1976).

    CAS  Google Scholar 

  34. Dore, J. E., Lukas, R., Sadler, D. W. & Karl, D. M. Climate-driven changes to the atmospheric CO2 sink in the subtropical North Pacific Ocean. Nature 424, 754–757 (2003).

    CAS  PubMed  Google Scholar 

  35. Dore, J. E., Lukas, R., Sadler, D. W., Church, M. J. & Karl, D. M. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. Proc. Natl Acad. Sci. USA 106, 12235–12240 (2009). This paper documents the progressive acidification of the upper portion of the North Pacific Ocean and highlights depth-dependent changes in rate of acidification, based on HOT programme measurements of the carbonate system at Station ALOHA. This paper was awarded the 2010 Cozzarelli Prize.

    CAS  PubMed  Google Scholar 

  36. Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1, 169–192 (2009).

    Google Scholar 

  37. Chisholm, S. W. et al. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334, 340–343 (1988).

    Google Scholar 

  38. Partensky, F., Hess, W. R. & Vaulot, D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Molec. Biol. Rev. 63, 106–127 (1999).

    CAS  Google Scholar 

  39. Campbell, L., Nolla, H. A. & Vaulot, D. The importance of Prochlorococcus to community structure in the central North Pacific Ocean. Limnol. Oceanogr. 39, 954–961 (1994). This is the first report of Prochlorococcus spp. at Station ALOHA in the NPSG.

    CAS  Google Scholar 

  40. Campbell, L., Liu, H. B., Nolla, H. A. & Vaulot, D. Annual variability of phytoplankton and bacteria in the subtropical North Pacific Ocean at Station ALOHA during the 1991–1994 ENSO event. Deep Sea Res. Part I 44, 167–192 (1997).

    CAS  Google Scholar 

  41. Moore, L. R., Rocap, G. & Chisholm, S. W. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393, 464–467 (1998).

    CAS  PubMed  Google Scholar 

  42. Bouman, H. A. et al. Oceanographic basis of the global surface distribution of Prochlorococcus ecotypes. Science 312, 918–921 (2006).

    CAS  PubMed  Google Scholar 

  43. Johnson, Z. I. et al. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311, 1737–1740 (2006).

    CAS  PubMed  Google Scholar 

  44. Malmstrom, R. R. et al. Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific Oceans. ISME J. 4, 1252–1264 (2010).

    PubMed  Google Scholar 

  45. Sher, D., Thompson, J. W., Kashtan, N., Croal, L. & Chisholm, S. W. Response of Prochlorococcus ecotypes to co-culture with diverse marine bacteria. ISME J. 5, 1125–1132 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Biller, S. J. et al. Bacterial vesicles in marine ecosystems. Science 343, 183–186 (2014).

    CAS  PubMed  Google Scholar 

  47. Dufresne, A. et al. Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc. Natl Acad. Sci. USA 100, 10020–10025 (2003).

    CAS  PubMed  Google Scholar 

  48. Coleman, M. L. & Chisholm, S. W. Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol. 15, 398–407 (2007).

    CAS  PubMed  Google Scholar 

  49. Kettler, G. C. et al. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet. 3, 2515–2528 (2007).

    CAS  Google Scholar 

  50. Coleman, M. L. & Chisholm, S. W. Ecosystem-specific selection pressures revealed through comparative population genomics. Proc. Natl Acad. Sci. USA 107, 18634–18639 (2010).

    CAS  PubMed  Google Scholar 

  51. Malmstrom, R. R. et al. Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis. ISME J. 7, 184–198 (2013).

    CAS  PubMed  Google Scholar 

  52. Flombaum, P. et al. Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl Acad. Sci. USA 110, 9824–9829 (2013).

    CAS  PubMed  Google Scholar 

  53. Schmidt, T. M., DeLong, E. F. & Pace, N. R. Analysis of a marine picoplankton community by 16S ribosomal-RNA cloning and sequencing. J. Bacteriol. 173, 4371–4378 (1991). This paper provides the first analyses of rRNA genes from marine plankton at Station ALOHA. Among other findings, this study identified genes that are derived from Prochlorococcus spp.and SAR11.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Giovannoni, S. J., Britschgi, T. B., Moyer, C. L. & Field, K. G. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345, 60–63 (1990).

    CAS  PubMed  Google Scholar 

  55. Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–810 (2002).

    CAS  PubMed  Google Scholar 

  56. Rappé, M. S., Connon, S. A., Vergin, K. L. & Giovannoni, S. J. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418, 630–633 (2002).

    PubMed  Google Scholar 

  57. Giovannoni, S. J. et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309, 1242–1245 (2005). This paper analyses the Ca . Pelagibacter ubique genome and reveals that the reduction of microbial genomes may be an important mechanism for survival in the oligotrophic open ocean.

    CAS  PubMed  Google Scholar 

  58. Grote, J. et al. Streamlining and core genome conservation among highly divergent members of the SAR11 clade. mBio 3, e00252-12 (2012).

    PubMed  PubMed Central  Google Scholar 

  59. Tripp, H. J. et al. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452, 741–744 (2008).

    CAS  PubMed  Google Scholar 

  60. Tripp, H. J. et al. Unique glycine-activated riboswitch linked to glycine-serine auxotrophy in SAR11. Environ. Microbiol. 11, 230–238 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Sun, J. et al. One carbon metabolism in SAR11 pelagic marine bacteria. PLoS ONE 6, e23973 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Carini, P., Steindler, L., Beszteri, S. & Giovannoni, S. J. Nutrient requirements for growth of the extreme oligotroph 'Candidatus Pelagibacter ubique' HTCC1062 on a defined medium. ISME J. 7, 592–602 (2012).

    PubMed  PubMed Central  Google Scholar 

  63. Tripp, H. J. The unique metabolism of SAR11 aquatic bacteria. J. Microbiol. 51, 147–153 (2013).

    CAS  PubMed  Google Scholar 

  64. Eiler, A., Hayakawa, D. H., Church, M. J., Karl, D. M. & Rappé, M. S. Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific subtropical gyre. Environ. Microbiol. 11, 2291–2300 (2009).

    CAS  PubMed  Google Scholar 

  65. Vergin, K. L. et al. High intraspecific recombination rate in a native population of Candidatus Pelagibacter ubique (SAR11). Environ. Microbiol. 9, 2430–2440 (2007).

    CAS  PubMed  Google Scholar 

  66. Joint, I. Unravelling the enigma of SAR11. ISME J. 2, 455–456 (2008).

    CAS  PubMed  Google Scholar 

  67. Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  69. Fuhrman, J. A., McCallum, K. & Davis, A. A. Novel major archaebacterial group from marine plankton. Nature 356, 148–149 (1992). References 68 and 69 are the first reports of planktonic archaea in the sea.

    CAS  PubMed  Google Scholar 

  70. Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nature Rev. Microbiol. 6, 245–252 (2008).

    CAS  Google Scholar 

  71. Pester, M., Schleper, C. & Wagner, M. The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 14, 300–306 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. DeLong, E. F., Taylor, L. T., Marsh, T. L. & Preston, C. M. Visualization and enumeration of marine planktonic archaea and bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl. Environ. Microbiol. 65, 5554–5563 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001). This paper quantifies the numerical dominance of archaea in the deep sea, based on FISH cell enumerations of planktonic bacteria and archaea.

    CAS  PubMed  Google Scholar 

  74. Preston, C. M., Wu, K. Y., Molinski, T. F. & DeLong, E. F. A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc. Natl Acad. Sci. USA 93, 6241–6246 (1996).

    CAS  PubMed  Google Scholar 

  75. Hallam, S. J. et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4, e95 (2006).

    PubMed  PubMed Central  Google Scholar 

  76. Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005).

    PubMed  Google Scholar 

  77. Walker, C. B. et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl Acad. Sci. USA 107, 8818–8823 (2010).

    CAS  PubMed  Google Scholar 

  78. Béjà, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000). This paper documents the initial discovery of proteorhodopsin genes among marine bacteria and demonstrates the functional role of this light-driven proton pump.

    PubMed  Google Scholar 

  79. Béjà, O., Spudich, E. N., Spudich, J. L., Leclerc, M. & DeLong, E. F. Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789 (2001).

    PubMed  Google Scholar 

  80. Karl, D. M. Solar energy capture and transformation in the sea. Elementa http://dx.doi.org/10.12952/journal.elementa.000021 (2014).

  81. de la Torre, J. R. et al. Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proc. Natl Acad. Sci. USA 100, 12830–12835 (2003).

    CAS  PubMed  Google Scholar 

  82. Fuhrman, J. A., Schwalbach, M. S. & Stingl, U. Proteorhodopsins: an array of physiological roles? Nature Rev. Microbiol. 6, 488–494 (2008).

    CAS  Google Scholar 

  83. 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).

    CAS  PubMed  Google Scholar 

  84. Walter, J. M., Greenfield, D., Bustamante, C. & Liphardt, J. Light-powering Escherichia coli with proteorhodopsin. Proc. Natl Acad. Sci. USA 104, 2408–2412 (2007).

    CAS  PubMed  Google Scholar 

  85. Goméz-Consarnau, L. et al. Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation. PLoS Biol. 8, e1000358 (2010).

    PubMed  PubMed Central  Google Scholar 

  86. Steindler, L., Schwalbach, M. S., Smith, D. P., Chan, F. & Giovannoni, S. J. Energy starved Candidatus Pelagibacter ubique substitutes light-mediated ATP production for endogenous carbon respiration. PLoS ONE 6, e19725 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Goméz-Consarnau, L. et al. Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445, 210–213 (2007). This study was the first to document that proteorhodopsin confers physiological advantages to marine bacteria.

    PubMed  Google Scholar 

  88. Kimura, H., Young, C. R., Martinez, A. & DeLong, E. F. Light-induced transcriptional responses associated with proteorhodopsin-enhanced growth in a marine flavobacterium. ISME J. 5, 1641–1651 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Kolber, Z. S., Van Dover, C. L., Niederman, R. A. & Falkowski, P. G. Bacterial photosynthesis in surface waters of the open ocean. Nature 407, 177–179 (2000).

    CAS  PubMed  Google Scholar 

  90. Kolber, Z. S. et al. Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292, 2492–2495 (2001).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  92. Béjà, O. et al. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415, 630–633 (2002).

    PubMed  Google Scholar 

  93. Frias-Lopez, J. et al. Microbial community gene expression in ocean surface waters. Proc. Natl Acad. Sci. USA 105, 3805–3810 (2008). This study, which was conducted at Station ALOHA, is one of the first metatranscriptomic studies of ocean microorganisms and highlights the apparent importance of various phototrophic and chemotrophic pathways of obtaining energy.

    CAS  PubMed  Google Scholar 

  94. Kirchman, D. L. & Hanson, T. E. Bioenergetics of photoheterotrophic bacteria in the oceans. Environ. Microbiol. Rep. 5, 188–199 (2013).

    CAS  PubMed  Google Scholar 

  95. Williams, P. J. le B. On the definition of plankton production terms. ICES Mar. Sci. Symp. 197, 9–19 (1993).

    Google Scholar 

  96. Karl, D. M. et al. Seasonal and interannual variability in primary production and particle flux at Station ALOHA. Deep Sea Res. Part II 43, 539–568 (1996).

    CAS  Google Scholar 

  97. Karl, D. M., Church, M. J., Dore, J. E., Letelier, R. M. & Mahaffey, C. Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc. Natl Acad. Sci. USA 109, 1842–1849 (2012). Based on a 12 year record of particle flux to the deep sea, this paper documents the coupled interactions between microorganism growth and metabolism in the upper ocean and the flux of material and energy to the deep sea.

    CAS  PubMed  Google Scholar 

  98. Quay, P. D. et al. Measuring primary production rates in the ocean: enigmatic results between incubation and non-incubation methods at Station ALOHA. Global Biogeochem. Cycles 24, GB3014 (2010).

    Google Scholar 

  99. Eppley, R. W. & Peterson, B. J. The flux of particulate organic matter to the deep ocean and its relation to planktonic new production. Nature 282, 677–680 (1979). This paper presents a new paradigm that couples new production to particulate matter export in the sea.

    Google Scholar 

  100. Johnson, K. S., Riser, S. C. & Karl, D. M. Nitrate supply from deep to near-surface waters of the North Pacific subtropical gyre. Nature 465, 1062–1065 (2010). This study documents the frequency and magnitude of episodic injections of nitrate into the lower euphotic zone in the NPSG using profiling floats equipped with autonomous nutrient sensors.

    CAS  PubMed  Google Scholar 

  101. Karl, D. M., Letelier, R., Hebel, D. V., Bird, D. F. & Winn, C. D. in Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (eds Carpenter, E. J. & Capone, D. G.) 219–237 (Kluwer Academic Publishers, 1992).

    Google Scholar 

  102. Ascani, F. et al. Physical and biological controls of nitrate concentrations in the upper subtropical North Pacific Ocean. Deep Sea Res. Part II 93, 119–134 (2013).

    CAS  Google Scholar 

  103. Duce, R. A. et al. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320, 893–897 (2008).

    CAS  PubMed  Google Scholar 

  104. Karl, D. M. et al. in Nitrogen in the Marine Environment (eds Capone, D. G., Bronk, D. A., Mulholland, M. R. & Carpenter, E. J.), 705–759 (Academic Press, 2008).

    Google Scholar 

  105. Von Brand, T., Rakestraw, N. W. & Renn, C. The experimental decomposition and regeneration of nitrogenous organic matter in sea water. Biol. Bull. 72, 165–175 (1937).

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  109. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311, 496–503 (2006). This paper highlights the importance of vertical gradients in the ocean habitat in structuring microbial communities and function using depth-resolved metagenomic sequencing at Station ALOHA.

    CAS  PubMed  Google Scholar 

  110. Mincer, T. J. et al. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9, 1162–1175 (2007).

    CAS  PubMed  Google Scholar 

  111. Konstantinidis, K. T., Braff, J., Karl, D. M. & DeLong, E. F. Comparative metagenomic analysis of a microbial community residing at a depth of 4,000 meters at Station ALOHA in the North Pacific Subtropical Gyre. Appl. Environ. Microbiol. 75, 5345–5355 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Church, M. J., Wai, B., Karl, D. M. & DeLong, E. F. Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean. Environ. Microbiol. 12, 679–688 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Dore, J. E. & Karl, D. M. Nitrification in the euphotic zone as a source for nitrite, nitrate and nitrous oxide at Station ALOHA. Limnol. Oceanogr. 41, 1619–1628 (1996).

    CAS  Google Scholar 

  114. Dore, J. E., Popp, B. N., Karl, D. M. & Sansone, F. J. A large source of atmospheric nitrous oxide from subtropical North Pacific surface waters. Nature 396, 63–66 (1998). Using an isotope-based approach, this paper highlights the important role of nitrification in producing the potent greenhouse gas nitrous oxide in the subtropical North Pacific Ocean.

    CAS  Google Scholar 

  115. Beman, J. M. et al. Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc. Natl Acad. Sci. USA 108, 208–213 (2011).

    CAS  PubMed  Google Scholar 

  116. Martens-Habbena, W., Berube, P. M., Urakawa, H., De La Torre, J. R. & Stahl, D. A. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461, 976–979 (2009).

    CAS  PubMed  Google Scholar 

  117. Santoro, A. E. & Casciotti, K. L. Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. ISME J. 5, 1796–1808 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Dore, J. E. & Karl, D. M. Nitrite distributions and dynamics at Station ALOHA. Deep Sea Res. Part II 43, 385–402 (1996).

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  121. Carpenter, E. J. & Capone, D. G. (eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs (Kluwer Academic Publishers, 1992).

    Google Scholar 

  122. Zehr, J. P. et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412, 635–638 (2001).

    CAS  PubMed  Google Scholar 

  123. Grabowski, M. N. W., Church, M. J. & Karl, D. M. Nitrogen fixation rates and controls at Stn ALOHA. Aquat. Microb. Ecol. 52, 175–183 (2008).

    Google Scholar 

  124. Church, M. J. et al. Physical forcing of nitrogen fixation and diazotroph community structure in the North Pacific subtropical gyre. Global Biogeochem. Cycles 23, GB2020 (2009). This paper presents a synthesis of multiple data sets from Station ALOHA and a model for the environmental and climate controls on N 2 fixation.

    Google Scholar 

  125. Zehr, J. P., Bench, S. R., Mondragon, E. A., McCarren, J. & DeLong, E. F. Low genomic diversity in tropical oceanic N2-fixing cyanobacteria. Proc. Natl Acad. Sci. USA 104, 17807–17812 (2007).

    CAS  PubMed  Google Scholar 

  126. Zehr, J. P. et al. Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322, 1110–1112 (2008). This paper reports the surprising discovery that widely distributed and abundant unicellular N 2 -fixing cyanobacteria lack the genetic capacity for inorganic carbon fixation and oxygen-evolving photosynthesis.

    CAS  PubMed  Google Scholar 

  127. Tripp, H. J. et al. Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 464, 90–94 (2010).

    CAS  PubMed  Google Scholar 

  128. Thompson, A. W. et al. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337, 1546–1550 (2012).

    CAS  PubMed  Google Scholar 

  129. Church, M. J., Jenkins, B. D., Karl, D. M. & Zehr, J. P. Vertical distributions of nitrogen-fixing phylotypes at Stn ALOHA in the oligotrophic North Pacific Ocean. Aquat. Microb. Ecol. 38, 3–14 (2005).

    Google Scholar 

  130. Church, M. J., Short, C. M., Jenkins, B. D., Karl, D. M. & Zehr, J. P. Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl. Environ. Microbiol. 71, 5362–5370 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  131. Mohr, W., Grosskopf, T., Wallace, D. W. R. & LaRoche, J. Methodological underestimation of oceanic nitrogen fixation rates. PLoS ONE 5, e12583 (2010).

    PubMed  PubMed Central  Google Scholar 

  132. Wilson, S. T., Bottjer, D., Church, M. J. & Karl, D. M. Comparative assessment of nitrogen fixation methodologies, conducted in the oligotrophic North Pacific Ocean. Appl. Environ. Microbiol. 78, 6516–6523 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Dugdale, R. C. & Goering, J. J. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol. Oceanogr. 12, 196–206 (1967). This paper presents the new production hypothesis that stimulated subsequent field research on nutrient control of primary production.

    CAS  Google Scholar 

  134. Karl, D. M. A new source of 'new' nitrogen in the sea. Trends Microbiol. 8, 301 (2000).

    CAS  PubMed  Google Scholar 

  135. Karl, D. et al. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538 (1997). Using time series measurements from Station ALOHA, this paper documents coupled linkages between N 2 fixation and the cycling of other bioelements in the ocean and quantifies the importance of N 2 fixation in ecosystem productivity and export.

    CAS  Google Scholar 

  136. 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. Part II 48, 1449–1470 (2001).

    Google Scholar 

  137. Sherwood, O. A., Guilderson, T. P., Batista, F. C., Schiff, J. T. & McCarthy, M. D. Increasing subtropical North Pacific Ocean nitrogen fixation since the Little Ice Age. Nature 505, 78–81 (2014).

    PubMed  Google Scholar 

  138. Van Mooy, B. A. S. et al. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458, 69–72 (2009).

    CAS  PubMed  Google Scholar 

  139. Björkman, K. M. & Karl, D. M. Bioavailability of dissolved organic phosphorus in the euphotic zone at Station ALOHA, North Pacific Subtropical Gyre. Limnol. Oceanogr. 48, 1049–1057 (2003).

    Google Scholar 

  140. Karl, D. M. Microbially-mediated transformations of phosphorus in the sea: new views of an old cycle. Ann. Rev. Mar. Sci. 6, 279–337 (2014).

    PubMed  Google Scholar 

  141. Karl, D. M. & Björkman, K. M. in Biogeochemistry of Marine Dissolved Organic Matter (eds Hansell, D. & Carlson, C.) 249–366 (Academic Press, 2002).

    Google Scholar 

  142. McGrath, J. W., Chin, J. P. & Quinn, J. P. Organophosphates revealed: new insights into the microbial metabolism of ancient molecules. Nature Rev. Microbiol. 11, 412–419 (2013).

    CAS  Google Scholar 

  143. Clark, L. L., Ingall, E. D. & Benner, R. Marine phosphorus is selectively remineralized. Nature 393, 426 (1998).

    CAS  Google Scholar 

  144. Kolowith, L. C., Ingall, E. D. & Benner, R. Composition and cycling of marine organic phosphorus. Limnol. Oceanogr. 46, 309–320 (2001).

    CAS  Google Scholar 

  145. Villareal-Chiu, J. F., Quinn, J. P. & McGrath, J. W. The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment. Front. Microbiol. 3, 1–13 (2012).

    Google Scholar 

  146. White, A. K. & Metcalf, W. W. Microbial metabolism of reduced phosphorus compounds. Annu. Rev. Microbiol. 61, 379–400 (2007).

    CAS  PubMed  Google Scholar 

  147. Karl, D. M. et al. Aerobic production of methane in the sea. Nature Geosci. 1, 473–478 (2008).

    CAS  Google Scholar 

  148. Beversdorf, L. J., White, A. E., Björkman, K. M., Letelier, R. M. & Karl, D. M. Phosphonate metabolism of Trichodesmium IMS101 and the production of greenhouse gases. Limnol. Oceanogr. 55, 1768–1778 (2010).

    CAS  Google Scholar 

  149. Metcalf, W. W. et al. Synthesis of methylphosphonic acid by marine microbes: a source of methane in the aerobic ocean. Science 337, 1104–1107 (2012). This paper describes the genetic pathways underlying the synthesis of methylphosphonic acid by the marine archaeon N. maritimus ; it highlights a potential source of methlyphosphonates to the marine environment and provides support for the hypothesis that the aerobic consumption of methylphosphonates by marine bacteria fuels the observed supersaturation of methane in the sea.

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Carini, P., White, A. E., Campbell, E. O. & Giovannoni, S. J. Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria. Nature Commun. 5, 4346 (2014).

    CAS  Google Scholar 

  151. Duarte, C. M., Cebrián, J. & Marbà, N. Uncertainty of detecting sea change. Nature 356, 190 (1992).

    Google Scholar 

  152. Rudnick, D. L. & Davis, R. E. Red noise and regime shifts. Deep Sea Res. Part I 50, 691–699 (2003).

    Google Scholar 

  153. Wunsch, C. The interpretation of short climate records, with comments on the North Atlantic and Southern oscillations. Bull. Amer. Meteorol. Soc. 80, 245–255 (1999).

    Google Scholar 

  154. Carpenter, S. R. et al. Early warnings of regime shifts: a whole-ecosystem experiment. Science 332, 1079–1082 (2011).

    CAS  PubMed  Google Scholar 

  155. Henson, S. A. et al. Detection of anthropogenic climate change in satellite records of ocean chlorophyll and productivity. Biogeosciences 7, 621–640 (2010).

    CAS  Google Scholar 

  156. Beaulieu, C. et al. Factors challenging our ability to detect long-term trends in ocean chlorophyll. Biogeosciences 10, 2711–2724 (2013).

    Google Scholar 

  157. Ottesen, E. A. et al. Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science 345, 207–212 (2014).

    CAS  PubMed  Google Scholar 

  158. Carpenter, S. R., Folke, C., Scheffer, M. & Westley, F. Resilience: accounting for the noncomputable. Ecol. Soc. 14, 13 (2009).

    Google Scholar 

  159. Crick, F. H. On protein synthesis. Symp. Soc. Exp. Biol. 12, 139–163 (1958). This paper is a benchmark in the history of science — a must read.

    Google Scholar 

  160. Maxam, A. M. & Gilbert, W. A new method for sequencing DNA. Proc. Natl Acad. Sci. USA 74, 560–564 (1977).

    CAS  PubMed  Google Scholar 

  161. Sanger, F., Nicklen, S. & Coulson, A. R. DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA 74, 5463–5467 (1977).

    CAS  PubMed  Google Scholar 

  162. Fleischmann, R. D. et al. Whole-genome random sequencing and assembly of Haemophilus influenza Rd. Science 269, 496–512 (1995).

    CAS  PubMed  Google Scholar 

  163. Stepanauskas, R. & Sieracki, M. E. Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proc. Natl Acad. Sci. USA 104, 9052–9057 (2007).

    CAS  PubMed  Google Scholar 

  164. Pace, N. R. A molecular view of microbial diversity and the biosphere. Science 276, 734–740 (1997). This seminal paper presents a new view of microbial diversity based on cultivation-independent analysis of 16S RNA genes.

    CAS  PubMed  Google Scholar 

  165. 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).

    CAS  PubMed  Google Scholar 

  166. Pedrós-Alió, C. The rare bacterial biosphere. Annu. Rev. Mar. Sci. 4, 449–466 (2012).

    Google Scholar 

  167. Amaral-Zettler, L. et al. in Life in the World's Oceans: Diversity, Distribution, and Abundance (ed. McIntyre, A.), 223–245 (Wiley-Blackwell, 2010).

    Google Scholar 

  168. Rusch, D. B. et al. The Sorcerer II global ocean sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5, e77 (2007).

    PubMed  PubMed Central  Google Scholar 

  169. McCarren, J. et al. Microbial community transcritomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc. Natl Acad. Sci. USA 107, 16420–16427 (2010).

    CAS  PubMed  Google Scholar 

  170. Shilova, I. N. et al. A microarray for assessing transcription from pelagic marine microbial taxa. ISME J. 8, 1476–1491 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  171. Scholin, C. A. in Encyclopedia of Biodiversity 2nd edn (ed. Levin, S. A.) 690–700 (Academic Press, 2013).

    Google Scholar 

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Acknowledgements

The authors acknowledge the US National Science Foundation (NSF) for sustained support of the Hawaii Ocean Time-series (HOT) programme (including the current grant OCE1260164). In addition, funding from the NSF to the Center for Microbial Oceanography: Research and Education (C-MORE) (grant EF0424599), the Gordon and Betty Moore Foundation (Marine Microbiology Investigator #3794), the Agouron Institute and the Simons Foundation to the Simons Collaboration on Ocean Processes and Ecology (SCOPE) support research at Station ALOHA (A Long-term Oligotrophic Habitat Assessment). They also acknowledge the dedicated efforts of the HOT team, including researchers, students, postdoctoral researchers and staff, who have all made important contributions to the HOT programme.

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  1. Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaii, 1950 East-West Road, Honolulu, 96822, Hawaii, USA

    David M. Karl & Matthew J. Church

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Correspondence to David M. Karl.

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Glossary

Gyres

The vast ecosystems that encompass open ocean waters of the tropical and subtropical regions of the oceans. The circular movements of the gyres, deriving from the combination of wind stress on the sea surface and the rotation of the Earth, result in physically isolated, stratified upper ocean waters that are persistently devoid of bioessential inorganic nutrients.

Biome

Contiguous habitats that share similar biogeochemical and physical properties.

Oligotrophic

A term used to describe environments that are characterized by low concentrations of growth-requiring nutrients and, consequently, low microbial biomass. Such habitats dominate the upper ocean of the large subtropical gyres. An oligotroph is the term used to describe an organism that is adapted to growing in habitats with low-nutrient conditions.

Euphotic zone

The region of the well-lit upper ocean that sustains the net production of organic matter. Often defined by the depth of penetration of sunlight, typically the depth to which 0.1 % of the light intensity that is observed at the surface ocean penetrates. In clear, open ocean ecosystems, the euphotic zone can extend to 150–200 m.

Climatology

In oceanography, this term refers to the determination of the mean ecosystem state, which requires averaging of time-resolved observations of sufficient duration to adequately sample processes underlying the dominant modes of ecosystem variability.

Primary production

The synthesis of organic matter from inorganic carbon. In the ocean, the vast majority of primary production is fuelled by photosynthesis.

Mesoscale eddies and Rossby waves

Physical processes that occur at spatial scales of 50–500 km and generally persist for 10–100 days. Such processes can originate from instability in the flow of currents owing to topographic features, variations in wind stress at the surface of the ocean or result from shear in the flow of waters of differing physical properties (that is, viscosity and density), such as along frontal boundaries. Such physical perturbations can propagate energy through the ocean in the form of waves or can result in the formation of isolated circulation vortices (similar to a cyclone in the atmosphere) that horizontally transport water of similar physical properties.

Biogeochemistry

The study of the interactions between biological processes and geochemical properties on Earth.

Phycobiliproteins

Proteins that are found in the photosynthetic light-harvesting complexes of various phototrophic cyanobacteria and eukaryotic algae. The proteins capture light energy and, via fluorescence events, transfer energy to photosynthetic reaction centres.

Genetic microadaptation

Selective evolutionary changes in the genetic content of closely related microorganisms.

Chemolithoautotrophic

A term used to describe organisms that use sources of chemical energy, rely on inorganic compounds (for example, H2O and H2S) for reducing power and assimilate inorganic carbon for cellular growth.

Proteorhodopsin

A photoactive, transmembrane protein that functions as a light-driven proton pump. Different forms of the protein differ in their light-absorption characteristics, which enables the absorption of light energy from different regions of the visible light spectrum. In the ocean, proteorhodopsin is found among diverse members of the Bacteria, Archaea and Eukarya.

Copiotrophic

A term used to describe an organism that is adapted to growth in habitats where nutrient concentrations are high. Such habitats are rare in the open sea but can occur at microscales, such as those in proximity to sources of organic matter (that is, living cells and detritus).

Mesopelagic

A term used to describe the vertical region of the ocean that encompasses the mid-depth (generally ∼ 200–1000 m) waters that lie between the well-lit euphotic zone and the deep bathypelagic waters. The mesopelagic waters are characterized by vanishingly low light and pronounced gradients in temperature and nutrients.

Diazotroph

A dinitrogen (N2)-fixing microorganism. The ocean contains diverse assemblages of diazotrophs, which include microscopic single-celled organisms and larger filamentous forms. These organisms rely on diverse metabolisms and are frequently found in symbiosis with other planktonic prokaryotes and eukaryotes. Diazotrophs seem to be most abundant in the upper ocean, where nutrient concentrations (specifically inorganic nitrogen) are low and sunlight, which is their primary energy source, is plentiful.

Stoichiometry

The proportions of specific nutrient elements that are found in organic compounds or dissolved in seawater. Variance in the relative proportions of these elements provides insights into specific ecological and biogeochemical processes; for example, nitrogen fixation supplies fixed cells with nitrogen but consumes phosphorus from seawater, which results in a shift in the relative proportions of these two elements in cellular material and in seawater.

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Karl, D., Church, M. Microbial oceanography and the Hawaii Ocean Time-series programme. Nat Rev Microbiol 12, 699–713 (2014). https://doi.org/10.1038/nrmicro3333

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