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Microbial niches in marine oxygen minimum zones

Nature Reviews Microbiology volume 16, pages 723–729 (2018)Cite this article

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An Author Correction to this article was published on 08 October 2018

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Abstract

In the ocean’s major oxygen minimum zones (OMZs), oxygen is effectively absent from sea water and life is dominated by microorganisms that use chemicals other than oxygen for respiration. Recent studies that combine advanced genomic and chemical detection methods are delineating the different metabolic niches that microorganisms can occupy in OMZs. Understanding these niches, the microorganisms that inhabit them, and their influence on marine biogeochemical cycles is crucial as OMZs expand with increasing seawater temperatures.

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Fig. 1: Global marine OMZ distribution.

Reproduced from Frank J. Stewart and Osvaldo Ulloa, from: Metagenomics of the Microbial Nitrogen Cycle: Theory, Methods and Applications (Edited by: Diana Marco). Caister Academic Press, UK (2014)82.

Fig. 2: Chemical and biological gradients in OMZs.
Fig. 3: A diversity of metabolic niches in OMZs.

Change history

  • 08 October 2018

    In Figure  3, ‘Candidatus Scalindua’ and Thaumarchaeota were erroneously shown to produce nitrous oxide (N2O). As neither group directly produces N2O, the arrows and products have been removed both online and in the pdf. The authors apologize for any confusion caused.

References

  1. Thamdrup, B., Dalsgaard, T. & Revsbech, N. P. Widespread functional anoxia in the oxygen minimum zone of the Eastern South Pacific. Deep Sea Res. Part I Oceanogr. Res. Pap. 65, 36–45 (2012).

    Article  CAS  Google Scholar 

  2. Wishner, K. F., Outram, D. M., Seibel, B. A., Daly, K. L. & Williams, R. L. Zooplankton in the eastern tropical north Pacific: boundary effects of oxygen minimum zone expansion. Deep Sea Res. Part I Oceanogr. Res. Pap. 79, 122–140 (2013).

    Article  CAS  Google Scholar 

  3. Wright, J. J., Konwar, K. M. & Hallam, S. J. Microbial ecology of expanding oxygen minimum zones. Nat. Rev. Microbiol. 10, 381–394 (2012).

    Article  CAS  Google Scholar 

  4. Loginova, A. N., Thomsen, S. & Engel, A. Chromophoric and fluorescent dissolved organic matter in and above the oxygen minimum zone off Peru. J. Geophys. Res. Oceans. 121, 7973–7990 (2016).

    Article  CAS  Google Scholar 

  5. Cavan, E. L., Trimmer, M., Shelley, F. & Sanders, R. Remineralization of particulate organic carbon in an ocean oxygen minimum zone. Nat. Commun. 8, 14847 (2017).

    Article  CAS  Google Scholar 

  6. Aldunate, M., De la Iglesia, R., Bertagnolli, A. D. & Ulloa, O. Oxygen modulates bacterial community composition in the coastal upwelling waters off central Chile. Deep Sea Res. Part II Top. Stud. Oceanogr. https://doi.org/10.1016/j.dsr2.2018.02.001 (2018).

    Article  Google Scholar 

  7. Loscher, C. R. et al. Water column biogeochemistry of oxygen minimum zones in the eastern tropical North Atlantic and eastern tropical South Pacific oceans. Biogeosciences 13, 3585–3606 (2016).

    Article  Google Scholar 

  8. 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  CAS  Google Scholar 

  9. Schmidtko, S., Stramma, L. & Visbeck, M. Decline in global oceanic oxygen content during the past five decades. Nature 542, 335–339 (2017).

    Article  CAS  Google Scholar 

  10. Revsbech, N. P. et al. Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnol. Oceanogr. Meth. 7, 371–381 (2009).

    Article  CAS  Google Scholar 

  11. Revsbech, N. P., Thamdrup, B., Dalsgaard, T. & Canfield, D. E. Construction of stox oxygen sensors and their application for determination of O2 concentrations in oxygen minimum zones. Methods Enzymol. 486, 325–341 (2011).

    Article  CAS  Google Scholar 

  12. Larsen, M. et al. In situ quantification of ultra-low O2 concentrations in oxygen minimum zones: application of novel optodes. Limnol. Oceanogr. Meth. 14, 784–800 (2016).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Tiano, L. et al. Oxygen distribution and aerobic respiration in the north and south eastern tropical Pacific oxygen minimum zones. Deep Sea Res. Part I Oceanogr. Res. Pap. 94, 173–183 (2014).

    Article  CAS  Google Scholar 

  15. Dalsgaard, T. et al. Oxygen at nanomolar levels reversibly suppresses process rates and gene expression in anammox and denitrification in the oxygen minimum zone off Northern Chile. mBio 5, e01966 (2014).

    Article  CAS  Google Scholar 

  16. 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  CAS  Google Scholar 

  17. Suter, E. A., Pachiadaki, M., Taylor, G. T., Astor, Y. & Edgcomb, V. P. Free-living chemoautotrophic and particle-attached heterotrophic prokaryotes dominate microbial assemblages along a pelagic redox gradient. Environ. Microbiol. 20, 693–712 (2018).

    Article  CAS  Google Scholar 

  18. Bristow, L. A. et al. Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters. Proc. Natl Acad. Sci. USA 113, 10601–10606 (2016).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  20. Garcia-Robledo, E. et al. Cryptic oxygen cycling in anoxic marine zones. Proc. Natl Acad. Sci. USA. 114, 8319–8324 (2017).

    Article  CAS  Google Scholar 

  21. Zakem, E. J. & Follows, M. J. A theoretical basis for a nanomolar critical oxygen concentration. Limnol. Oceanogr. 62, 795–805 (2017).

    Article  CAS  Google Scholar 

  22. Bristow, L. A. et al. N2 production rates limited by nitrite availability in the Bay of Bengal oxygen minimum zone. Nat. Geosci. 10, 24–29 (2017).

    Article  CAS  Google Scholar 

  23. Resplandy, L. et al. Controlling factors of the oxygen balance in the Arabian Sea’s OMZ. Biogeosciences 9, 5095–5109 (2012).

    Article  CAS  Google Scholar 

  24. Goericke, R., Olson, R. J. & Shalapyonok, A. A novel niche for Prochlorococcus sp in low-light suboxic environments in the Arabian Sea and the Eastern Tropical North Pacific. Deep Sea Res. Part I Oceanogr. Res. Pap. 47, 1183–1205 (2000).

    Article  Google Scholar 

  25. Lavin, P., Gonzalez, B., Santibanez, J. F., Scanlan, D. J. & Ulloa, O. Novel lineages of Prochlorococcus thrive within the oxygen minimum zone of the eastern tropical South Pacific. Environ. Microbiol. Rep. 2, 728–738 (2010).

    Article  CAS  Google Scholar 

  26. Franz, J. et al. Dynamics and stoichiometry of nutrients and phytoplankton in waters influenced by the oxygen minimum zone in the eastern tropical Pacific. Deep Sea Res. Part I Oceanogr. Res. Pap. 62, 20–31 (2012).

    Article  CAS  Google Scholar 

  27. Astorga-Elo, M., Ramirez-Flandes, S., DeLong, E. F. & Ulloa, O. Genomic potential for nitrogen assimilation in uncultivated members of Prochlorococcus from an anoxic marine zone. ISME J. 9, 1264–1267 (2015).

    Article  CAS  Google Scholar 

  28. Sansone, F. J., Popp, B. N., Gasc, A., Graham, A. W. & Rust, T. M. Highly elevated methane in the eastern tropical North Pacific and associated isotopically enriched fluxes to the atmosphere. Geophys. Res. Lett. 28, 4567–4570 (2001).

    Article  CAS  Google Scholar 

  29. Naqvi, S. W. A. et al. Marine hypoxia/anoxia as a source of CH4 and N2O. Biogeosciences 7, 2159–2190 (2010).

    Article  CAS  Google Scholar 

  30. Chronopoulou, P. M., Shelley, F., Pritchard, W. J., Maanoja, S. T. & Trimmer, M. Origin and fate of methane in the Eastern Tropical North Pacific oxygen minimum zone. ISME J. 11, 1386–1399 (2017).

    Article  CAS  Google Scholar 

  31. Pack, M. A. et al. Methane oxidation in the eastern tropical North Pacific Ocean water column. J. Geophys. Res. Biogeo. 120, 1078–1092 (2015).

    Article  CAS  Google Scholar 

  32. Tavormina, P. L. et al. Abundance and distribution of diverse membrane-bound monooxygenase (Cu-MMO) genes within the Costa Rica oxygen minimum zone. Environ. Microbiol. Rep. 5, 414–423 (2013).

    Article  CAS  Google Scholar 

  33. Padilla, C. C. et al. Metagenomic binning recovers a transcriptionally active gammaproteobacterium linking methanotrophy to partial denitrification in an anoxic oxygen minimum zone. Front. Mar. Sci. https://doi.org/10.3389/fmars.2017.00023 (2017).

    Article  Google Scholar 

  34. Torres-Beltrán, M. et al. Methanotrophic community dynamics in a seasonally anoxic fjord: Saanich Inlet, British Columbia. Front. Mar. Sci. https://doi.org/10.3389/fmars.2016.00268 (2016).

    Article  Google Scholar 

  35. Padilla, C. C. et al. NC10 bacteria in marine oxygen minimum zones. ISME J. 10, 2067–2071 (2016).

    Article  CAS  Google Scholar 

  36. Ettwig, K. F. et al. Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ. Microbiol. 10, 3164–3173 (2008).

    Article  CAS  Google Scholar 

  37. Raghoebarsing, A. A. et al. A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440, 918–921 (2006).

    Article  CAS  Google Scholar 

  38. Reed, D. C., Algar, C. K., Huber, J. A. & Dick, G. J. Gene-centric approach to integrating environmental genomics and biogeochemical models. Proc. Natl Acad. Sci. USA 111, 1879–1884 (2014).

    Article  CAS  Google Scholar 

  39. 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  CAS  Google Scholar 

  40. Walsh, D. A. et al. Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science 326, 578–582 (2009).

    Article  CAS  Google Scholar 

  41. Hawley, A. K., Brewer, H. M., Norbeck, A. D., Pasa-Tolic, L. & Hallam, S. J. Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes. Proc. Natl Acad. Sci. USA 111, 11395–11400 (2014).

    Article  CAS  Google Scholar 

  42. Murillo, A. A., Ramírez-Flandes, S., DeLong, E. F. & Ulloa, O. Enhanced metabolic versatility of planktonic sulfur-oxidizing γ-proteobacteria in an oxygen-deficient coastal ecosystem. Front. Mar. Sci. https://doi.org/10.3389/fmars.2014.00018 (2014).

    Article  Google Scholar 

  43. Shah, V., Chang, B. X. & Morris, R. M. Cultivation of a chemoautotroph from the SUP05 clade of marine bacteria that produces nitrite and consumes ammonium. ISME J. 11, 263–271 (2017).

    Article  CAS  Google Scholar 

  44. Callbeck, C. M. et al. Oxygen minimum zone cryptic sulfur cycling sustained by offshore transport of key sulfur oxidizing bacteria. Nat. Commun. 9, 1729 (2018).

    Article  Google Scholar 

  45. Giovannoni, S. J. SAR11 Bacteria: the most abundant plankton in the oceans. Annu. Rev. Mar. Sci. 9, 231–255 (2017).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  47. Tsementzi, D. et al. SAR11 bacteria linked to ocean anoxia and nitrogen loss. Nature 536, 179–183 (2016).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  49. Kashtan, N. et al. Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344, 416–420 (2014).

    Article  CAS  Google Scholar 

  50. Bryant, J. A., Stewart, F. J., Eppley, J. M. & DeLong, E. F. Microbial community phylogenetic and trait diversity declines with depth in a marine oxygen minimum zone. Ecology 93, 1659–1673 (2012).

    Article  Google Scholar 

  51. Beman, J. M. & Carolan, M. T. Deoxygenation alters bacterial diversity and community composition in the ocean’s largest oxygen minimum zone. Nat. Commun. 4, 2705 (2013).

    Article  Google Scholar 

  52. Cassman, N. et al. Oxygen minimum zones harbour novel viral communities with low diversity. Environ. Microbiol. 14, 3043–3065 (2012).

    Article  CAS  Google Scholar 

  53. Woebken, D. et al. A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ. Microbiol. 10, 3106–3119 (2008).

    Article  CAS  Google Scholar 

  54. Luke, C., Speth, D. R., Kox, M. A. R., Villanueva, L. & Jetten, M. S. M. Metagenomic analysis of nitrogen and methane cycling in the Arabian Sea oxygen minimum zone. PeerJ 4, e1924 (2016).

    Article  Google Scholar 

  55. Villanueva, L., Speth, D. R., van Alen, T., Hoischen, A. & Jetten, M. S. M. Shotgun metagenomic data reveals significant abundance but low diversity of “Candidatus Scalindua” marine anammox bacteria in the Arabian Sea oxygen minimum zone. Front. Microbiol. https://doi.org/10.3389/fmicb.2014.00031 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Ganesh, S. et al. Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria. ISME J. https://doi.org/10.1038/s41396-018-0223-9 (2018).

    Article  PubMed  Google Scholar 

  57. Babbin, A. R. et al. Multiple metabolisms constrain the anaerobic nitrite budget in the Eastern Tropical South Pacific. Global Biogeochem. Cycles 31, 258–271 (2017).

    CAS  Google Scholar 

  58. Bianchi, D., Babbin, A. R. & Galbraith, E. D. Enhancement of anammox by the excretion of diel vertical migrators. Proc. Natl Acad. Sci. USA 111, 15653–15658 (2014).

    Article  CAS  Google Scholar 

  59. Fernandez, C., Gonzalez, M. L., Munoz, C., Molina, V. & Farias, L. Temporal and spatial variability of biological nitrogen fixation off the upwelling system of central Chile (35–38.5 °S). J. Geophys. Res. Oceans 120, 3330–3349 (2015).

    Article  CAS  Google Scholar 

  60. Bonnet, S. et al. Dynamics of N-2 fixation and fate of diazotroph-derived nitrogen in a low-nutrient, low-chlorophyll ecosystem: results from the VAHINE mesocosm experiment (New Caledonia). Biogeosciences 13, 2653–2673 (2016).

    Article  CAS  Google Scholar 

  61. Jayakumar, A. et al. Biological nitrogen fixation in the oxygen-minimum region of the eastern tropical North Pacific ocean. ISME J. 11, 2356–2367 (2017).

    Article  CAS  Google Scholar 

  62. Loescher, C. R. et al. Facets of diazotrophy in the oxygen minimum zone waters off Peru. ISME J. 8, 2180–2192 (2014).

    Article  CAS  Google Scholar 

  63. Martinez-Perez, C. et al. Metabolic versatility of a novel N2-fixing Alphaproteobacterium isolated from a marine oxygen minimum zone. Environ. Microbiol. 20, 755–768 (2018).

    Article  CAS  Google Scholar 

  64. Delmont, T. O. et al. Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes. Nat. Microbiol. 3, 804–813 (2018).

    Article  CAS  Google Scholar 

  65. Thrash, J. C. et al. Metabolic roles of uncultivated bacterioplankton lineages in the northern Gulf of Mexico “dead zone”. mBio 8, e01017–17 (2017).

    Article  Google Scholar 

  66. Hawley, A. K. et al. Diverse Marinimicrobia bacteria may mediate coupled biogeochemical cycles along eco-thermodynamic gradients. Nat. Commun. 8, 1507 (2017).

    Article  Google Scholar 

  67. Georges, A. A., El-Swais, H., Craig, S. E., Li, W. K. W. & Walsh, D. A. Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton. ISME J. 8, 1301–1313 (2014).

    Article  CAS  Google Scholar 

  68. Bertagnolli, A. D., Padilla, C. C., Glass, J. B., Thamdrup, B. & Stewart, F. J. Metabolic potential and in situ activity of marine Marinimicrobia bacteria in an anoxic water column. Environ. Microbiol. 19, 4392–4416 (2017).

    Article  CAS  Google Scholar 

  69. Sheik, C. S., Jain, S. & Dick, G. J. Metabolic flexibility of enigmatic SAR324 revealed through metagenomics and metatranscriptomics. Environ. Microbiol. 16, 304–317 (2014).

    Article  CAS  Google Scholar 

  70. Marshall, K. T. & Morris, R. M. Genome sequence of “Candidatus Thioglobus singularis” strain PS1, a mixotroph from the SUP05 clade of marine gammaproteobacteria. Genome Announc. 3, e01155–15 (2015).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  72. Widner, B. & Mulholland, M. R. Cyanate distribution and uptake in North Atlantic coastal waters. Limnol. Oceanogr. 62, 2538–2549 (2017).

    Article  CAS  Google Scholar 

  73. Glass, J. B. et al. Meta-omic signatures of microbial metal and nitrogen cycling in marine oxygen minimum zones. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.00998 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  74. 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  CAS  Google Scholar 

  75. Hawco, N. J., Ohnemus, D. C., Resing, J. A., Twining, B. S. & Saito, M. A. A dissolved cobalt plume in the oxygen minimum zone of the eastern tropical South Pacific. Biogeosciences 13, 5697–5717 (2016).

    Article  CAS  Google Scholar 

  76. Qin, W. et al. Influence of oxygen availability on the activities of ammonia-oxidizing archaea. Environ. Microbiol. Rep. 9, 250–256 (2017).

    Article  CAS  Google Scholar 

  77. Grote, J. et al. Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones. Proc. Natl Acad. Sci. USA 109, 506–510 (2012).

    Article  CAS  Google Scholar 

  78. Henson, M. W. et al. Artificial seawater media facilitate cultivating members of the microbial majority from the Gulf of Mexico. mSphere https://doi.org/10.1128/mSphere.00028-16 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Mok, J. K. et al. Iodate reduction by Shewanella oneidensis does not involve nitrate reductase. Geomicrobiol. J. 35, 570–579 (2018).

    Article  CAS  Google Scholar 

  80. Fussel, J. et al. Nitrite oxidation in the Namibian oxygen minimum zone. ISME J. 6, 1200–1209 (2012).

    Article  Google Scholar 

  81. Fussel, J. et al. Adaptability as the key to success for the ubiquitous marine nitrite oxidizer Nitrococcus. Sci. Adv. 3, e1700807 (2017).

    Article  Google Scholar 

  82. Stewart, F. J. & Ulloa, O. in Metagenomics of the Microbial Nitrogen Cycle: Theory, Methods and Applications (ed. Marco, D.) 17–31 (Caister Academic Press, 2014).

  83. Peng, X. F. et al. Ammonia and nitrite oxidation in the Eastern Tropical North Pacific. Global. Biogeochem. Cy. 29, 2034–2049 (2015).

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank the National Science Foundation (grants 1151698, 1558916 and 1564559 to F.J.S.) for generous and valuable support of OMZ research.

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Nature Reviews Microbiology thanks A. Babbin, M. Kuypers and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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  1. School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA

    Anthony D. Bertagnolli & Frank J. Stewart

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Both authors researched data for the article, made substantial contributions to discussions of the content, wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to Frank J. Stewart.

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Bertagnolli, A.D., Stewart, F.J. Microbial niches in marine oxygen minimum zones. Nat Rev Microbiol 16, 723–729 (2018). https://doi.org/10.1038/s41579-018-0087-z

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