Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally

Abstract

The discovery of chemosynthetic ecosystems at deep-sea hydrothermal vents in 1977 changed our view of biology. Chemosynthetic bacteria and archaea form the foundation of vent ecosystems by exploiting the chemical disequilibrium between reducing hydrothermal fluids and oxidizing seawater, harnessing this energy to fix inorganic carbon into biomass. Recent research has uncovered fundamental aspects of these microbial communities, including their relationships with underlying geology and hydrothermal geochemistry, interactions with animals via symbiosis and distribution both locally in various habitats within vent fields and globally across hydrothermal systems in diverse settings. Although ‘black smokers’ and symbioses between microorganisms and macrofauna attract much attention owing to their novelty and the insights they provide into life under extreme conditions, habitats such as regions of diffuse flow, subseafloor aquifers and hydrothermal plumes have important roles in the global cycling of elements through hydrothermal systems. Owing to sharp contrasts in physical and chemical conditions between these various habitats and their dynamic, extreme and geographically isolated nature, hydrothermal vents provide a valuable window into the environmental and ecological forces that shape microbial communities and insights into the limits, origins and evolution of microbial life.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Global distribution of hydrothermal-vent systems.
Fig. 2: Microbial habitats at deep-sea hydrothermal vents.
Fig. 3: Generalized characteristics of vents.
Fig. 4: Ecological and biogeochemical interactions at deep-sea hydrothermal vents from a microbial perspective.

References

  1. Baker, M. C. et al. in Life in the World’s Oceans: Diversity, Distribution, and Abundance (ed. McIntyre, A. D.) 161–182 (Blackwell Publishing Ltd., 2010).

  2. Dick, G. J. Genomic Approaches in Earth and Environmental Sciences (Wiley Blackwell, 2018).

  3. Nakamura, K. & Takai, K. Theoretical constraints of physical and chemical properties of hydrothermal fluids on variations in chemolithotrophic microbial communities in seafloor hydrothermal systems. Prog. Earth Plan. Sci. 1, 5 (2014).

    Article  Google Scholar 

  4. Baas Becking, L. Geobiologie of Inleiding Tot de Milieukunde [Dutch] (Den Haag: W. P. Van Stockum & Zoon, 1934).

  5. Reysenbach, A. L., Banta, A. B., Boone, D. R., Cary, S. C. & Luther, G. W. Microbial essentials at hydrothermal vents. Nature 404, 835 (2000). This paper highlights the importance of microenvironments in defining microbial niches along the steep chemical gradients that are found at hydrothermal vents.

    Article  CAS  PubMed  Google Scholar 

  6. Kelley, D. S., Baross, J. A. & Delaney, J. R. Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Ann. Rev. Earth Plan. Sci. 30, 385–491 (2002). This is a comprehensive and thorough review of the fundamentals of geology, geochemistry and biology of mid-ocean ridge spreading centres.

    Article  CAS  Google Scholar 

  7. Orcutt, B. N., Sylvan, J. B., Knab, N. J. & Edwards, K. J. Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol. Mol. Biol. Rev. 75, 361–422 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Karl, D. M. The Microbiology of Deep-Sea Hydrothermal Vents (CRC Press, 1995).

  9. Sievert, S. M. & Vetriani, C. Chemoautotrophy at deep-sea vents past, present, and future. Oceanography 25, 218–233 (2012). This paper critically reviews the current understanding and knowledge gaps regarding the physiology and metabolism of chemoautotrophs at deep-sea hydrothermal vents.

    Article  Google Scholar 

  10. Edwards, K. J., Wheat, C. G. & Sylvan, J. B. Under the sea: microbial life in volcanic oceanic crust. Nat. Rev. Microbiol. 9, 703–712 (2011).

    Article  CAS  PubMed  Google Scholar 

  11. Dick, G. J. et al. Hydrothermal vent plume microbiology: ecological and biogeographic linkages to seafloor and water column habitats. Front. Microbiol. 4, 124 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Anantharaman, K., Breier, J. A. & Dick, G. J. Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center. ISME J. 10, 225–239 (2016).

    Article  CAS  PubMed  Google Scholar 

  13. Fortunato, C. S., Larson, B., Butterfield, D. A. & Huber, J. A. Spatially distinct, temporally stable microbial populations mediate biogeochemical cycling at and below the seafloor in hydrothermal vent fluids. Environ. Microbiol. 20, 769–784 (2018). This study is a good example of how a combination of molecular and geochemical approaches can provide insights into how metabolic functions are distributed across different microbial groups and how the distribution of microorganisms and metabolisms is linked to hydrothermal chemistry.

    Article  CAS  PubMed  Google Scholar 

  14. Stetter, K. O. Extremophiles and their adaptation to hot environments. FEBS Lett. 452, 22–25 (1999).

    Article  CAS  PubMed  Google Scholar 

  15. Takai, K. et al. Cell proliferation at 122 degrees C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl Acad. Sci. USA 105, 10949–10954 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kashefi, K. & Lovley, D. R. Extending the upper temperature limit for life. Science 301, 934 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. Mora, M., Bellack, A., Ugele, M., Hopf, J. & Wirth, R. The temperature gradient-forming device, an accessory unit for normal light microscopes to study the biology of hyperthermophilic microorganisms. Appl. Environ. Microbiol. 80, 4764–4770 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Reysenbach, A. L. & Shock, E. Merging genomes with geochemistry in hydrothermal ecosystems. Science 296, 1077–1082 (2002).

    Article  CAS  PubMed  Google Scholar 

  19. Prieur, D., Erauso, G. & Jeanthon, C. Hyperthermophilic life at deep-sea hydrothermal vents. Planet. Space Sci. 43, 115–122 (1995).

    Article  CAS  PubMed  Google Scholar 

  20. Tuttle, J. H., Wirsen, C. O. & Jannasch, H. W. Microbial activities in the emitted hydrothermal waters of the Galapagos Rift vents. Mar. Biol. 73, 293–299 (1983).

    Article  Google Scholar 

  21. Wirsen, C. O., Tuttle, J. H. & Jannasch, H. W. Activities of sulfur-oxidizing bacteria at the 21N East Pacific Rise vent site. Mar. Biol. 92, 449–456 (1986).

    Article  CAS  Google Scholar 

  22. Reveillaud, J. et al. Subseafloor microbial communities in hydrogen-rich vent fluids from hydrothermal systems along the Mid-Cayman Rise. Environ. Microbiol. 18, 1970–1987 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Takai, K., Nakagawa, S., Reysenbach, A. L. & Hoek, J. in Back-Arc Spreading Systems: Geological, Biological, Chemical and Physical Interactions Vol. 166 (eds Christie, D. M., Fisher, C. R., Lee, S. M. & Givens, S.) 185–213 (American Geophysical Union, 2006).

  24. Amend, J. P., McCollom, T. M., Hentscher, M. & Bach, W. Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types. Geochim. Cosmochim. Acta 75, 5736–5748 (2011).

    Article  CAS  Google Scholar 

  25. Takai, K. & Nakamura, K. in Geomicrobiology: Molecular and Environmental Perspective (eds Loy, A., Mandl, M. & Barton, L. L.) 251–283 (Springer Netherlands, 2010).

  26. McCollum, T. M. Geochemical constraints on primary productivity in submarine hydrothermal vent plumes. Deep Sea Res. Part I Oceanogr. Res. Pap. 47, 85–101 (2000).

    Article  Google Scholar 

  27. McCollom, T. M. & Shock, E. L. Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim. Cosmochim. Acta 61, 4375–4391 (1997).

    Article  CAS  PubMed  Google Scholar 

  28. Reed, D. C. et al. Predicting the response of the deep-ocean microbiome to geochemical perturbations by hydrothermal vents. ISME J. 9, 1857–1869 (2015). This study shows how coupled hydrodynamic and thermodynamic models, in tandem with microbiological and physical oceanographic observations, can be used to understand the source, transport and growth of microorganisms in hydrothermal plumes.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  30. Nunoura, T. et al. A primordial and reversible TCA cycle in a facultatively chemolithoautotrophic thermophile. Science 359, 559–563 (2018).

    Article  CAS  PubMed  Google Scholar 

  31. Goffredi, S. et al. Inorganic carbon acquisition by the hydrothermal vent tubeworm Riftia pachyptila depends upon high external PCO2 and upon proton-equivalent ion transport by the worm. J. Exp. Biol. 200, 883–896 (1997).

    Article  CAS  PubMed  Google Scholar 

  32. Schrenk, M. O., Kelley, D. S., Bolton, S. A. & Baross, J. A. Low archaeal diversity linked to subseafloor geochemical processes at the lost city hydrothermal field, Mid-Atlantic Ridge. Environ. Microbiol. 6, 1086–1095 (2004).

    Article  CAS  PubMed  Google Scholar 

  33. Mangiapia, M. et al. Proteomic and mutant analysis of the CO2 concentrating mechanism of hydrothermal vent chemolithoautotroph thiomicrospira crunogena. J. Bacteriol. 199, e00871–16 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Johnson, K. S., Childress, J. J. & Beehler, C. L. Short-term temperature variability in the rose garden hydrothermal vent field - an unstable deep-sea environment. Deep Sea Res. A 35, 1711–1721 (1988).

    Article  Google Scholar 

  35. Campbell, B. J., Summers Engel, A., Porter, M. L. & Takai, K. The versatile ε-proteobacteria: key players in sulphidic habitats. Nat. Rev. Microbiol. 4, 458–468 (2006).

    Article  CAS  PubMed  Google Scholar 

  36. Koschinsky, A. et al. Hydrothermal venting at pressure-temperature conditions above the critical point of seawater, 5°S on the Mid-Atlantic Ridge. Geology 36, 615 (2008).

    Article  CAS  Google Scholar 

  37. McDermott, J., Sylva, S. P., Ono, S., German, C. R. & Seewald, J. S. Geochemistry of fluids from Earth’s deepest ridge-crest hot-springs: Piccard hydrothermal field, Mid-Cayman Rise. Geochim. Cosmochim. Acta 228, 95–118 (2018).

    Article  CAS  Google Scholar 

  38. LaRowe, D. E. et al. Modeling micorbial reaction rates in a submarine hydrothermal vent chimney wall. Geochim. Cosmochim. Acta 124, 72–97 (2014).

    Article  CAS  Google Scholar 

  39. Tivey, M. K. in The Subseafloor Biosphere at Mid-Ocean Ridges (eds Wilcock, W. S. D., DeLong, E. F., Kelley, D. S., Baross, J. A. & Cary, S. C.) 137–152 (American Geophysical Union, 2004).

  40. Flores, G. E. et al. Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin. Geobiology 10, 333–346 (2012).

    Article  CAS  PubMed  Google Scholar 

  41. Takai, K. et al. Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field. Extremophiles 8, 269–282 (2004).

    Article  CAS  PubMed  Google Scholar 

  42. Brazelton, W. J., Nelson, B. & Schrenk, M. O. Metagenomic evidence for H2 oxidation and H2 production by serpentine-hosted subsurface microbial communities. Front. Microbiol. 2, 268 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Wirth, R. Colonization of black smokers by hyperthermophilic microorganisms. Trends Microbiol. 25, 92–99 (2017).

    Article  CAS  PubMed  Google Scholar 

  44. Huber, R., Stoffers, P., Cheminee, J. L., Richnow, H. H. & Stetter, K. O. Hyperthermophilic archaebacteria within the crater and open-sea plume of erupting Macdonald Seamount. Nature 345, 179–182 (1990).

    Article  Google Scholar 

  45. Gonnella, G. et al. Endemic hydrothermal vent species identified in the open ocean seed bank. Nat. Microbiol. 1, 16086 (2016). This study presents evidence that taxa previously thought to be endemic to deep-sea hydrothermal vents are, in fact, present in ambient deep seawater, suggesting frequent dispersal of vent microorganisms between geographically distant vent sites.

    Article  CAS  PubMed  Google Scholar 

  46. Langseth, M. G., Becker, K., Herzen, R. P. V. & Schultheiss, P. Heat and fluid flux through sediment on the western flank of the Mid-Atlantic Ridge: a hydrogeological study of North Pond. Geophys. Res. Lett. 19, 517–520 (1992).

    Article  Google Scholar 

  47. Huber, J. A. & Holden, J. F. in Magma to Microbe: Modeling Hydrothermal Processes at Ocean Spreading Centers (eds Lowell, R. P., Seewald, J. S., Metaxas, A. & Perfit, M. R.) 215–231 (American Geophysical Union, 2008).

  48. McCollom, T. M. Energetic constraints on subsurface biomass production within igneous ocean crust. Geochem. Cosmochim. Acta 69, A200 (2005).

    Google Scholar 

  49. Cowen, J. P. et al. Fluids from aging ocean crust that support microbial life. Science 299, 120–123 (2003).

    Article  CAS  PubMed  Google Scholar 

  50. Santelli, C. M. et al. Abundance and diversity of microbial life in ocean crust. Nature 453, 653–656 (2008).

    Article  CAS  PubMed  Google Scholar 

  51. Walter, S. R. S. et al. Microbial decomposition of marine dissolved organic matter in cool oceanic crust. Nat. Geosci. 11, 334–339 (2018).

    Article  CAS  Google Scholar 

  52. Schrenk, M. O., Huber, J. A. & Edwards, K. J. Microbial provinces in the subseafloor. Ann. Rev. Earth Plan. Sci. 2, 279–304 (2010).

    Google Scholar 

  53. Ishibashi, J., Okino, K. & Sunamura, M. Subseafloor Biosphere Linked to Hydrothermal Systems (Springer, Tokyo, 2015).

  54. Huber, J. A., Butterfield, D. A. & Baross, J. A. Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiol. Ecol. 43, 393–409 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Perner, M. et al. In situ chemistry and microbial community compositions in five deep-sea hydrothermal fluid samples from Irina II in the Logatchev field. Environ. Microbiol. 15, 1551–1560 (2013).

    Article  CAS  PubMed  Google Scholar 

  56. Huber, J. A., Butterfield, D. A. & Baross, J. A. Temporal changes in archaeal diversity and chemistry in a mid-ocean ridge subseafloor habitat. Appl. Environ. Microbiol. 68, 1585–1594 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Vetriani, C. et al. Deep-sea hydrothermal vent epsilonproteobacteria encode a conserved and widespread nitrate reduction pathway (Nap). ISME J. 8, 1510–1521 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Burggraf, S., Jannasch, H. W., Nicolaus, B. & Stetter, K. O. Archaeoglobus profundus sp. nov., represents a new species within the sulfate-reducing Archaebacteria. Syst. Appl. Microbiol. 13, 24–28 (1990).

    Article  Google Scholar 

  59. Deming, J. A. & Baross, J. A. Deep-sea smokers: windows to a subsurface biosphere? Geochim. Cosmochim. Acta 57, 3219–3230 (1993).

    Article  CAS  PubMed  Google Scholar 

  60. Holden, J. F. & Adams, M. W. Microbe-metal interactions in marine hydrothermal environments. Curr. Opin. Chem. Biol. 7, 160–165 (2003).

    Article  CAS  PubMed  Google Scholar 

  61. Juniper, S. K., Martineu, P., Sarrazin, J. & Gelinas, Y. Microbial-mineral floc associated with nascent hydrothermal activity on coaxial segment, Juan-De-Fuca Ridge. Geophys. Res. Lett. 22, 179–182 (1995).

    Article  CAS  Google Scholar 

  62. Moussard, H., Corre, E., Cambon-Bonavita, M. A., Fouquet, Y. & Jeanthon, C. Novel uncultured Epsilonproteobacteria dominate a filamentous sulphur mat from the 13 degrees N hydrothermal vent field, East Pacific Rise. FEMS Microbiol. Ecol. 58, 449–463 (2006).

    Article  CAS  PubMed  Google Scholar 

  63. Sievert, S. M., Hugler, M., Taylor, C. D. & Wirsen, C. O. in Microbial Sulfur Metabolism (eds Dahl, C. & Friedrich, C. G.) 238–258 (Springer, 2008).

  64. Meyer, J. L., Akerman, N. H., Proskurowski, G. & Huber, J. A. Microbiological characterization of post-eruption “snowblower” vents at Axial Seamount, Juan de Fuca Ridge. Front. Microbiol. 4, 153 (2013).

    PubMed  PubMed Central  Google Scholar 

  65. Emerson, D. et al. A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLOS ONE 2, e667 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Girguis, P. R. & Lee, R. W. Thermal preference and tolerance of alvinellids. Science 312, 231 (2006).

    Article  PubMed  Google Scholar 

  67. Cary, S. C., Shank, T. & Stein, J. Worms bask in extreme temperatures. Nature 391, 545–546 (1998).

    Article  CAS  Google Scholar 

  68. Dubilier, N., Bergin, C. & Lott, C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6, 725–740 (2008).

    Article  CAS  PubMed  Google Scholar 

  69. Van Dover, C. L. The Ecology of Deep Sea Hydrothermal Vents (Princeton Univ. Press, 2000).

  70. Gardebrecht, A. et al. Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics. ISME J. 6, 766–776 (2012).

    Article  CAS  PubMed  Google Scholar 

  71. Robidart, J. C., Roque, A., Song, P. & Girguis, P. R. Linking hydrothermal geochemistry to organismal physiology: physiological versatility in Riftia pachyptila from sedimented and basalt-hosted vents. PLOS ONE 6, e21692 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Childress, J. J. & Girguis, P. R. The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities. J. Exp. Biol. 214, 312–325 (2011).

    Article  CAS  PubMed  Google Scholar 

  73. Van Dover, C. L. et al. Biogeography and ecological setting of Indian Ocean hydrothermal vents. Science 294, 818–823 (2001).

    Article  PubMed  Google Scholar 

  74. Petersen, J. M., Wentrup, C., Verna, C., Knittel, K. & Dubilier, N. Origins and evolutionary flexibility of chemosynthetic symbionts from deep-sea animals. Biol. Bull. 223, 123–137 (2012).

    Article  CAS  PubMed  Google Scholar 

  75. Bang, C. et al. Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127, 1–19 (2018).

    Article  PubMed  Google Scholar 

  76. Petersen, J. M. et al. Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476, 176–180 (2011).

    Article  CAS  PubMed  Google Scholar 

  77. Li, Y., Liles, M. R. & Halanych, K. M. Endosymbiont genomes yield clues of tubeworm success. ISME J. 12, 2785–2795 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Markert, S. et al. Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315, 247–250 (2007).

    Article  CAS  PubMed  Google Scholar 

  79. Robidart, J. C. et al. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ. Microbiol. 10, 727–737 (2008).

    Article  CAS  PubMed  Google Scholar 

  80. Stewart, F. J. & Cavanaugh, C. M. Symbiosis of thioautotrophic bacteria with Riftia pachyptila. Prog. Mol. Subcell. Biol. 41, 197–225 (2006).

    Article  CAS  PubMed  Google Scholar 

  81. Bright, M. & Bulgheresi, S. A complex journey: transmission of microbial symbionts. Nat. Rev. Microbiol. 8, 218–230 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Fisher, C. R., Brooks, J. M., Vodenichar, J. S., Zande, J. M. & Chidress, J. J. The co-occurrence of methanotrophic and chemoautotrophic sulfur-oxidizing bacterial symbionts in a deep-sea mussel. Mar. Ecol. 14, 277–289 (1993).

    Article  Google Scholar 

  83. Beinart, R. A. et al. Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses. Proc. Natl Acad. Sci. USA 109, E3241–E3250 (2012). This paper shows how microbial symbionts are linked to habitat partitioning of animals across different geochemical niches at deep-sea hydrothermal vents.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Sanders, J. G., Beinart, R. A., Stewart, F. J., Delong, E. F. & Girguis, P. R. Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J. 7, 1556–1567 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Goffredi, S. K. Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebrates. Environ. Microbiol. Rep. 2, 479–488 (2010).

    Article  PubMed  Google Scholar 

  86. Van Dover, C. L., Fry, B., Grassle, J. F., Humphris, S. & Rona, P. A. Feeding biology of the shrimp Rimicaris exoculata at hydrotheraml vents on the Mid-Atlantic Ridge. Mar. Biol. 98, 209–216 (1988).

    Article  Google Scholar 

  87. Watsuji, T. O. et al. Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri. ISME J. 9, 821–831 (2015).

    Article  CAS  PubMed  Google Scholar 

  88. Goffredi, S. K., Waren, A., Orphan, V. J., Van Dover, C. L. & Vrijenhoek, R. C. Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl. Environ. Microbiol. 70, 3082–3090 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Sayavedra, L. et al. Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels. eLife 4, e07966 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Lesniewski, R. A., Jain, S., Anantharaman, K., Schloss, P. D. & Dick, G. J. The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs. ISME J. 6, 2257–2268 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Baker, B. J., Lesniewski, R. A. & Dick, G. J. Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume. ISME J. 6, 2269–2279 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. 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  CAS  PubMed  Google Scholar 

  93. Dick, G. J. et al. Enzymatic microbial Mn(II) oxidation and Mn biooxide production in the Guaymas Basin hydrothermal plume. Geochim. Cosmochim. Acta 73, 6517–6530 (2009).

    Article  CAS  Google Scholar 

  94. Li, M. et al. Microbial iron uptake as a mechanism for dispersing iron from deep-sea hydrothermal vents. Nat. Commun. 6, 8933 (2014).

    Article  CAS  Google Scholar 

  95. Levin, L. A. et al. Hydrothermal vents and methane seeps: rethinking the sphere of influence. Front. Mar. Sci. 3, 72 (2016).

    Article  Google Scholar 

  96. Breier, J. A. et al. A large volume particulate and water multi-sampler with in situ preservation for microbial and biogeochemical studies. Deep Sea Res. Part I Oceanogr. Res. Pap. 94, 195–206 (2014).

    Article  CAS  Google Scholar 

  97. Dick, G. J. & Tebo, B. M. Microbial diversity and biogeochemistry of the Guaymas Basin deep-sea hydrothermal plume. Environ. Microbiol. 12, 1334–1347 (2010).

    Article  CAS  PubMed  Google Scholar 

  98. German, C. R. et al. Diverse styles of submarine venting on the ultraslow spreading Mid-Cayman Rise. Proc. Natl Acad. Sci. USA 107, 14020–14025 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Sheik, C. S. et al. Spatially resolved sampling reveals dynamic microbial communities in rising hydrothermal plumes across a back-arc basin. ISME J. 9, 1434–1445 (2015).

    Article  PubMed  Google Scholar 

  100. Sylvan, J. B., Pyenson, B. C., Rouxel, O., German, C. R. & Edwards, K. J. Time-series analysis of two hydrothermal plumes at 9 degrees 50’N East Pacific Rise reveals distinct, heterogeneous bacterial populations. Geobiology 10, 178–192 (2012).

    Article  CAS  PubMed  Google Scholar 

  101. Cowen, J. P. et al. Geomicrobial transformation of manganese in Gorda Ridge event plumes. Deep Sea Res. Part II Top. Stud. Oceanogr. 45, 2713–2738 (1998).

    Article  CAS  Google Scholar 

  102. Klose, J. et al. Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population. Proc. Natl Acad. Sci. USA 112, 11300–11305 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Summit, M. & Baross, J. A. A novel microbial habitat in the mid-ocean ridge subseafloor. Proc. Natl Acad. Sci. USA 98, 2158–2163 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Nakagawa, S. et al. Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ. Microbiol. 7, 1619–1632 (2005).

    Article  CAS  PubMed  Google Scholar 

  105. Opatkiewicz, A. D., Butterfield, D. A. & Baross, J. A. Individual hydrothermal vents at Axial Seamount harbor distinct subseafloor microbial communities. FEMS Microbiol. Ecol. 70, 413–424 (2009).

    Article  CAS  PubMed  Google Scholar 

  106. Huber, J. A. et al. Isolated communities of epsilonproteobacteria in hydrothermal vent fluids of the Mariana Arc seamounts. FEMS Microbiol. Ecol. 73, 538–549 (2010).

    CAS  PubMed  Google Scholar 

  107. Huber, J. A., Butterfield, D. A. & Baross, J. A. Diversity and distribution of subseafloor thermococcales populations in diffuse hydrothermal vents at an active deep-sea volcano in the northeast Pacific Ocean. J. Geophys. Res. Biogeosci. 111, G04016 (2006).

    Article  CAS  Google Scholar 

  108. Luther, G. W. III et al. Chemical speciation drives hydrothermal vent ecology. Nature 410, 813–816 (2001). This paper highlights the importance of chemical speciation, in this case, the availability of free sulfide, in structuring biological communities at deep-sea hydrothermal vents.

    Article  CAS  PubMed  Google Scholar 

  109. Larson, B. I., Houghton, J. L., Lowell, R. P., Farough, A. & Meile, C. D. Subsurface conditions in hydrothermal vents inferred from diffuse flow composition, and models of reaction and transport. Earth Planet. Sci. Lett. 424, 245–255 (2015).

    Article  CAS  Google Scholar 

  110. Perner, M. et al. The influence of ultramafic rocks on microbial communities at the Logatchev hydrothermal field, located 15 degrees N on the Mid-Atlantic Ridge. FEMS Microbiol. Ecol. 61, 97–109 (2007).

    Article  CAS  PubMed  Google Scholar 

  111. Ver Eecke, H. C. et al. Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents. Proc. Natl Acad. Sci. USA 109, 13674–13679 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Meier, D. V. et al. Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents. ISME J. 11, 1545–1558 (2017). This paper shows how the niches of sulfur-oxidizing bacteria are partitioned according to the chemical environment across small spatial and temporal scales.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  114. Corliss, J. B. et al. Submarine thermal springs on the Galapagos Rift. Science 203, 1073–1083 (1979). This paper describes the discovery of deep-sea hydrothermal-vent ecosystems and lays out the hypothesis that chemosynthesis is the main source of primary production.

    Article  CAS  PubMed  Google Scholar 

  115. Einen, J., Thorseth, I. H. & Ovreas, L. Enumeration of archaea and bacteria in seafloor basalt using real-time quantitative PCR and fluorescence microscopy. FEMS Microbiol. Lett. 282, 182–187 (2008).

    Article  CAS  PubMed  Google Scholar 

  116. Sylvan, J. B., Toner, B. M. & Edwards, K. J. Life and death of deep-sea vents: bacterial diversity and ecosystem succession on inactive hydrothermal sulfides. mBio 3, e00279–11 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Mino, S. et al. Endemicity of the cosmopolitan mesophilic chemolithoautotroph Sulfurimonas at deep-sea hydrothermal vents. ISME J. 11, 909–919 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506 (2012).

    Article  CAS  PubMed  Google Scholar 

  119. Kelley, D. S. et al. A serpentinite-hosted ecosystem: the Lost City hydrothermal field. Science 307, 1428–1434 (2005).

    Article  CAS  PubMed  Google Scholar 

  120. Mccollom, T. M. Geochemical constraints on sources of metabolic energy for chemolithoautotrophy in ultramafic-hosted deep-sea hydrothermal systems. Astrobiology 7, 933–950 (2007).

    Article  CAS  PubMed  Google Scholar 

  121. Flores, G. E. et al. Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. Environ. Microbiol. 13, 2158–2171 (2011).

    Article  CAS  PubMed  Google Scholar 

  122. German, C. R. et al. Hydrothermal impacts on trace element and isotope ocean biogeochemistry. Philos. Trans. A Math. Phys. Eng. Sci. 374, 20160035 (2016).

    PubMed  PubMed Central  Google Scholar 

  123. Sunamura, M. & Yanagawa, K. in Subseafloor Biosphere Linked to Hydrothermal Systems (eds Ishibashi, J., Okino, K. & Sunamura, M.) 31–38 (Springer, 2015).

  124. Mino, S. et al. Biogeography of persephonella in deep-sea hydrothermal vents of the Western Pacific. Front. Microbiol. 4, 107 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  125. Anderson, R. E., Sogin, M. L. & Baross, J. A. Biogeography and ecology of the rare and abundant microbial lineages in deep-sea hydrothermal vents. FEMS Microbiol. Ecol. 91, 1–11 (2015).

    Article  PubMed  CAS  Google Scholar 

  126. Ochman, H. & Wilson, A. C. Evolution in bacteria - evidence for a universal substitution rate in cellular genomes. J. Mol. Evol. 26, 74–86 (1987).

    Article  CAS  PubMed  Google Scholar 

  127. Girguis, P. Here, there and everywhere. Nat. Microbiol. 1, 16123 (2016).

    Article  CAS  PubMed  Google Scholar 

  128. Whitaker, R. J., Grogan, D. W. & Taylor, J. W. Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301, 976–978 (2003).

    Article  CAS  PubMed  Google Scholar 

  129. Govenar, B. Energy transfer through food webs at hydrothermal vents: linking the lithosphere to the biosphere. Oceanography 25, 246–255 (2012).

    Article  Google Scholar 

  130. Bennett, S. A. et al. Trophic regions of a hydrothermal plume dispersing away from an ultramafic-hosted vent-system: Von Damm vent-site, Mid-Cayman Rise. Geochem. Geophys. Geosyst. 14, 317–327 (2013).

    Article  CAS  Google Scholar 

  131. Beinart, R. A., Gartman, A., Sanders, J. G., Luther, G. W. & Girguis, P. R. The uptake and excretion of partially oxidized sulfur expands the repertoire of energy resources metabolized by hydrothermal vent symbioses. Proc. Biol. Sci. 282, 20142811 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Ortmann, A. C. & Suttle, C. A. High abundances of viruses in a deep-sea hydrothermal vent system indicates viral mediated microbial mortality. Deep Sea Res. Part I Oceanogr. Res. Pap. 52, 1515–1527 (2005).

    Article  Google Scholar 

  133. Yoshida-Takashima, Y. et al. Spatial distribution of viruses associated with planktonic and attached microbial communities in hydrothermal environments. Appl. Environ. Microbiol. 78, 1311–1320 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Suttle, C. A. Marine viruses - major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801–812 (2007).

    Article  CAS  PubMed  Google Scholar 

  135. Breitbart, M., Bonnain, C., Malki, K. & Sawaya, N. A. Phage puppet masters of the marine microbial realm. Nat. Microbiol. 3, 754–766 (2018).

    Article  CAS  PubMed  Google Scholar 

  136. Williamson, S. J. et al. Lysogenic virus-host interactions predominate at deep-sea diffuse-flow hydrothermal vents. ISME J. 2, 1112–1121 (2008).

    Article  CAS  PubMed  Google Scholar 

  137. Anantharaman, K. et al. Sulfur oxidation genes in diverse deep-sea viruses. Science 344, 757–760 (2014).

    Article  CAS  PubMed  Google Scholar 

  138. He, T. L., Li, H. Y. & Zhang, X. B. Deep-sea hydrothermal vent viruses compensate for microbial metabolism in virus-host interactions. mBio 8, e00893–17 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  139. Elderfield, H. & Schultz, A. Mid-ocean ridge hydrothermal fluxes and the chemical composition of the ocean. Ann. Rev. Earth Plan. Sci. 24, 191–224 (1996).

    Article  CAS  Google Scholar 

  140. Tagliabue, A. et al. Hydrothermal contribution to the oceanic dissolved iron inventory. Nat. Geosci. 3, 252–256 (2010).

    Article  CAS  Google Scholar 

  141. Fitzsimmons, J. N. et al. Iron persistence in a distal hydrothermal plume supported by dissolved-particulate exchange. Nat. Geosci. 10, 195–201 (2017).

    Article  CAS  Google Scholar 

  142. Toner, B. M. et al. Preservation of iron(II) by carbon-rich matrices in a hydrothermal plume. Nat. Geosci. 2, 197–201 (2009).

    Article  CAS  Google Scholar 

  143. Cowen, J. P., Massoth, G. J. & Baker, E. T. Bacterial scavenging of Mn and Fe in a mid- to far-field hydrothermal particle plume. Nature 322, 169–171 (1986).

    Article  CAS  Google Scholar 

  144. Feely, R. A., Trefry, J. H., Lebon, G. T. & German, C. R. The relationship between P/Fe and V/Fe ratios in hydrothermal precipitates and dissolved phosphate in seawater. Geophys. Res. Lett. 25, 2253–2256 (1998).

    Article  CAS  Google Scholar 

  145. German, C. R. & Von Damm, K. L. in Treatise on Geochemistry Vol. 6 (eds Holland, H. D. & Turekian, K. K.) 181–222 (2004). This paper presents an accessible review of geological and geochemical processes in mid-ocean ridge hydrothermal systems and the impact of hydrothermal vents on the biogeochemistry of the oceans.

  146. Kadko, D. An assessment of the effect of chemical scavenging within submarine hydrothermal plumes upon ocean geochemistry. Earth Plan. Sci. Lett. 120, 361–374 (1993).

    Article  CAS  Google Scholar 

  147. Wankel, S. D. et al. Influence of subsurface biosphere on geochemical fluxes from diffuse hydrothermal fluids. Nat. Geosci. 4, 461–468 (2011). This paper shows the importance of in situ measurements in quantifying geochemical fluxes at hydrothermal vents.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  149. Swan, B. K. et al. Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333, 1296–12300 (2011).

    Article  CAS  PubMed  Google Scholar 

  150. 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  PubMed  PubMed Central  Google Scholar 

  151. 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  PubMed  PubMed Central  Google Scholar 

  152. Dick, G. J. Embracing the mantra of modellers and synthesizing omics, experiments and models. Environ. Microbiol. Rep. 9, 18–20 (2017).

    Article  PubMed  Google Scholar 

  153. Nakajima, R. et al. Post-drilling changes in seabed landscape and megabenthos in a deep-sea hydrothermal system, the Iheya North field, Okinawa Trough. PLOS ONE 10, e0123095 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  154. Van Dover, C. L. et al. Scientific rationale and international obligations for protection of active hydrothermal vent ecosystems from deep-sea mining. Mar. Policy 90, 20–28 (2018).

    Article  Google Scholar 

  155. Boetius, A. & Haeckel, M. Mind the seafloor. Science 359, 34–36 (2018).

    Article  CAS  PubMed  Google Scholar 

  156. Lutz, R. A. & Kennish, M. J. Ecology of deep-sea hydrothermal vent communities: a review. Rev. Geophys. 31, 211–242 (1993).

    Article  Google Scholar 

  157. Lonsdale, P. Clustering of suspension feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep Sea Res. A 24, 857–858 (1977).

    Article  Google Scholar 

  158. Ballard, R. D. Notes on a major oceanographic find. Oceanus 20, 35–44 (1977).

    Google Scholar 

  159. Jannasch, H. W. & Wirsen, C. O. Chemosynthetic primary production at East Pacific sea floor spreading centers. Bioscience 29, 592–598 (1979). This paper describes initial microbiological experiments and evidence for chemosynthesis as the main mode of primary production in deep-sea hydrothermal-vent ecosystems.

    Article  CAS  Google Scholar 

  160. Jannasch, H. W. & Mottl, M. J. Geomicrobiology of deep-sea hydrothermal vents. Science 229, 717–725 (1985).

    Article  CAS  PubMed  Google Scholar 

  161. Cavanaugh, C. M., Gardiner, S. L., Jones, M. L., Jannasch, H. W. & Waterbury, J. B. Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213, 340–342 (1981).

    Article  CAS  PubMed  Google Scholar 

  162. Girguis, P. R. & Holden, J. F. On the potential for bioenergy and biofuels from hydrothermal vent microbes. Oceanography 25, 213–217 (2012).

    Article  Google Scholar 

  163. Martin, W., Baross, J., Kelley, D. & Russell, M. J. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814 (2008).

    Article  CAS  PubMed  Google Scholar 

  164. Corliss, J. B., Baross, J. A. & Hoffman, S. E. An hypothesis concerning the relationship between submarine hot springs and the origin of life on Earth. Oceanol. Acta 4, 59–69 (1981).

    Google Scholar 

  165. Baross, J. A. & Hoffman, S. E. Submarine hydrothermal vents and associated gradient environments as sites for origin and evolution of life. Orig. Life Evol. Biosph. 15, 327–345 (1985).

    Article  CAS  Google Scholar 

  166. Russell, M. J. & Hall, A. J. The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J. Geol. Soc. London 154, 377–402 (1997).

    Article  CAS  PubMed  Google Scholar 

  167. Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).

    Article  CAS  PubMed  Google Scholar 

  168. Dodd, M. S. et al. Evidence for early life in Earth’s oldest hydrothermal vent precipitates. Nature 543, 60–64 (2017).

    Article  CAS  PubMed  Google Scholar 

  169. Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Holden, J. F., Breier, J. A., Rogers, K. L., Schulte, M. D. & Toner, B. M. Biogeochemical processes at hydrothermal vents: microbes and minerals, bioenergetics, and carbon fluxes. Oceanography 25, 196–208 (2012).

    Article  Google Scholar 

  171. Mullineaux, L. S. et al. Exploring the ecology of deep-sea hydrothermal vents in a metacommunity framework. Front. Mar. Sci. 5, 49 (2018).

    Article  Google Scholar 

  172. Adams, D. K., Arellano, S. M. & Govenar, B. Larval dispersal: vent life in the water column. Oceanography 25, 256–268 (2012).

    Article  Google Scholar 

  173. Nakagawa, S. & Takai, K. Deep-sea vent chemoautotrophs: diversity, biochemistry, and ecological significance. FEMS Microbiol. Ecol. 65, 1–14 (2008).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author thanks C. German for input and S. Beaulieu for guidance about the map in figure 1. The author is grateful to the wonderful group of staff, graduate students, postdocs and collaborators who worked on vents with him and helped develop some of the ideas presented here: K. Anantharaman, B. Baker, S. Jain, R. Lesniewski, M. Li, D. Reed, C. Sheik, B. Toner and J. Breier. The Gordon and Betty Moore Foundation Marine Microbiology Initiative supported this research. The preparation of this manuscript was supported by an Alfred P. Sloan Foundation Fellowship in Ocean Sciences.

Reviewer information

Nature Reviews Microbiology thanks K. Takai and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gregory J. Dick.

Ethics declarations

Competing interests

The author declares no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Chemosynthesis

The use of chemical energy to fix inorganic carbon into organic carbon for microbial growth.

Microbial mats

Dense, macroscopic communities of microorganisms attached to a solid surface.

Chemolithoautotrophic growth

The growth of bacteria or archaea using an inorganic, chemical source of energy (for example, reduced forms of iron, sulfur, hydrogen and ammonia) to fix inorganic carbon into organic carbon.

Reductive tricarboxylic acid cycle

(rTCA). A metabolic pathway for carbon fixation in which two molecules of carbon dioxide are converted into acetyl coenzyme A; it uses most of the same enzymes as the oxidative tricarboxylic acid cycle but runs it in reverse by using three alternative enzymes: fumarate reductase, 2-oxoglutarate synthase and ATP citrate lyase.

Calvin–Benson–Bassham cycle

A carbon fixation pathway in which carbon dioxide is converted into glyceraldehyde-3-phosphate using the key enzyme Rubisco.

Wood–Ljungdahl pathway

A metabolic pathway for carbon fixation in which two molecules of carbon dioxide are converted into acetyl coenzyme A by the key enzyme carbon monoxide dehydrogenase–acetyl coenzyme A synthase.

Dicarboxylate–4-hydroxybutyrate pathway

A recently described carbon fixation pathway in archaea in which a molecule of bicarbonate (HCO3) is fixed onto acetyl coenzyme A via a combination of enzymes from the reductive tricarboxylic acid cycle and the 4-hydroxybutyrate part of the 3-hydroxypropionate–4-hydroxybutyrate cycle.

Black smokers

Hydrothermal vents that eject plumes of black suspended particles, chiefly iron sulfide minerals.

White smokers

Hydrothermal vents that eject plumes of white suspended mineral particles composed mainly of calcium, barium and silica.

Ultramafic

Relating to igneous rocks that have a very low silica content and very high content of magnesium and iron.

Denitrifying

A type of process in which nitrate is used as an electron acceptor for energy metabolism and is reduced to di-nitrogen gas (denitrification).

Mineral flocs

Flocculent materials sometimes emitted from hydrothermal vents, composed of fine mineral particles and often microbial biomass.

Trophosome

An internal organ in tubeworms used to host chemosynthetic symbiotic bacteria.

Autotrophy

The growth of an organism through the fixation of inorganic carbon into organic carbon.

Heterotrophy

A mode of organism growth in which exogenous organic carbon functions as the source of carbon.

Allopatric speciation

The evolutionary divergence of a population into distinct species due to geographic separation.

Thermohaline conveyor

The global circulation of water in the oceans, driven by density gradients due to differences in the temperature and salinity of water masses.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dick, G.J. The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat Rev Microbiol 17, 271–283 (2019). https://doi.org/10.1038/s41579-019-0160-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-019-0160-2

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing