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Diversity, ecology and evolution of Archaea

An Author Correction to this article was published on 19 May 2020

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Abstract

Compared to bacteria, our knowledge of archaeal biology is limited. Historically, microbiologists have mostly relied on culturing and single-gene diversity surveys to understand Archaea in nature. However, only six of the 27 currently proposed archaeal phyla have cultured representatives. Advances in genomic sequencing and computational approaches are revolutionizing our understanding of Archaea. The recovery of genomes belonging to uncultured groups from the environment has resulted in the description of several new phyla, many of which are globally distributed and are among the predominant organisms on the planet. In this Review, we discuss how these genomes, together with long-term enrichment studies and elegant in situ measurements, are providing insights into the metabolic capabilities of the Archaea. We also debate how such studies reveal how important Archaea are in mediating an array of ecological processes, including global carbon and nutrient cycles, and how this increase in archaeal diversity has expanded our view of the tree of life and early archaeal evolution, and has provided new insights into the origin of eukaryotes.

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Fig. 1: Archaeal genomic diversity.
Fig. 2: Archaeal ecological roles.
Fig. 3: Archaea metabolic potential.
Fig. 4: An updated archaeal tree of life.
Fig. 5: Diversity of archaeal MCR proteins.

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References

  1. Chatton, E. Titres et travaux scientifiques (1906–1937) de Edouard Chatton. (Sète: Impr. E. Sottan, 1938).

  2. Whittaker, R. H. New concepts of kingdoms of organisms. Science 163, 150–160 (1969).

    Article  CAS  PubMed  Google Scholar 

  3. Woese, C. R. et al. Conservation of primary structure in 16S ribosomal RNA. Nature 254, 83–86 (1975).

    Article  CAS  PubMed  Google Scholar 

  4. Balch, W. E., Magrum, L. J., Fox, G. E., Wolfe, R. S. & Woese, C. R. An ancient divergence among the bacteria. J. Mol. Evol. 9, 305–311 (1977).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Woese, C. R., Magrum, L. J. & Fox, G. E. Archaebacteria. J. Mol. Evol. 11, 245–251 (1978).

    Article  CAS  PubMed  Google Scholar 

  7. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Doolittle, W. F. & Logsdon, J. M. Jr. Archaeal genomics: do archaea have a mixed heritage? Curr. Biol. 8, R209–R211 (1998).

    Article  CAS  PubMed  Google Scholar 

  9. MacGregor, B. J., Moser, D. P., Alm, E. W., Nealson, K. H. & Stahl, D. A. Crenarchaeota in Lake Michigan sediment. Appl. Environ. Microbiol. 63, 1178–1181 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Olsen, G. Microbial ecology and evolution: a ribosomal RNA approach. Annu. Rev. Microbiol. 40, 337–365 (1986).

    Article  CAS  PubMed  Google Scholar 

  12. Rappé, M. S. & Giovannoni, S. J. The uncultured microbial majority. Annu. Rev. Microbiol. 57, 369–394 (2003).

    Article  PubMed  CAS  Google Scholar 

  13. Reysenbach, A. L., Giver, L. J., Wickham, G. S. & Pace, N. R. Differential amplification of rRNA genes by polymerase chain reaction. Appl. Environ. Microbiol. 58, 3417–3418 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hugenholtz, P., Goebel, B. M. & Pace, N. R. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180, 4765–4774 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Baker, B. J. & Dick, G. J. Omic approaches in microbial ecology: charting the unknown. Microbe 8, 353–359 (2013).

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  18. Barns, S. M., Fundgya, R. E., Jeffries, M. W. & Pace, N. R. Remarkable archaeal diversity detected in a Yellowstone national park hot spring environment. Proc. Natl Sci. USA 91, 1609–1613 (1994).

    Article  CAS  Google Scholar 

  19. Barns, S. M., Delwiche, C. F., Palmer, J. D. & Pace, N. R. Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc. Natl Acad. Sci. USA 93, 9188–9193 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Adam, P. S., Borrel, G., Brochier-Armanet, C. & Gribaldo, S. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J. 11, 2407–2425 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Peng, Y., Leung, H. C. M., Yiu, S. M. & Chin, F. Y. L. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428 (2012).

    Article  CAS  PubMed  Google Scholar 

  22. Tyson, G. W. et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43 (2004).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Dick, G. J. et al. Community-wide analysis of microbial genome sequence signatures. Genome Biol. 10, R85 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Dombrowski, N., Teske, A. P. & Baker, B. J. Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nat. Commun. 9, 4999 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).

    Article  CAS  PubMed  Google Scholar 

  28. Guy, L. & Ettema, T. J. G. The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580–587 (2011).

    Article  CAS  PubMed  Google Scholar 

  29. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).

    Article  CAS  PubMed  Google Scholar 

  30. Smith, P. H. & Hungate, R. E. Isolation and characterization of Methanobacterium ruminantium n. sp. J. Bacteriol. 75, 713–718 (1958).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Brock, T. D. & Darland, G. K. Limits of microbial existence: temperature and pH. Science 169, 1316–1318 (1970).

    Article  CAS  PubMed  Google Scholar 

  32. Fox, G. E., Magrum, L. J., Balch, W. E., Wolfe, R. S. & Woese, C. R. Classification of methanogenic bacteria by 16S ribosomal RNA characterization. Proc. Natl Acad. Sci. USA 74, 4537–4541 (1977).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wolfe, R. S. Microbial formation of methane. Adv. Microb. Physiol. 6, 107–146 (1971).

    Article  CAS  PubMed  Google Scholar 

  34. Larsen, H. Halophilic and halotolerant microorganisms-an overview and historical perspective. FEMS Microbiol. Lett. 2, 3–7 (1986).

    Article  Google Scholar 

  35. Andrei, A.-Ş., Banciu, H. L. & Oren, A. Living with salt: metabolic and phylogenetic diversity of archaea inhabiting saline ecosystems. FEMS Microbiol. Lett. 330, 1–9 (2012).

    Article  CAS  PubMed  Google Scholar 

  36. Klenk, H. P. et al. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390, 364–370 (1997).

    Article  CAS  PubMed  Google Scholar 

  37. Takai, K. et al. Cell proliferation at 122 °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 

  38. Orphan, V. J., House, C. H., Hinrichs, K.-U., McKeegan, K. D. & DeLong, E. F. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc. Natl Acad. Sci. USA 99, 7663–7668 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wang, Y., Wegener, G., Hou, J., Wang, F. & Xiao, X. Expanding anaerobic alkane metabolism in the domain of Archaea. Nat. Microbiol. 4, 595–602 (2019).

    Article  CAS  PubMed  Google Scholar 

  40. Vetriani, C., Reysenbach, A. L. & Doré, J. Recovery and phylogenetic analysis of archaeal rRNA sequences from continental shelf sediments. FEMS Microbiol. Lett. 161, 83–88 (1998).

    Article  CAS  PubMed  Google Scholar 

  41. Iverson, V. et al. Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335, 587–590 (2012).

    Article  CAS  PubMed  Google Scholar 

  42. Needham, D. M. & Fuhrman, J. A. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat. Microbiol. 1, 16005 (2016).

    Article  CAS  PubMed  Google Scholar 

  43. Baker, B. J. et al. Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea. Nat. Microbiol. 1, 16002 (2016).

    Article  CAS  PubMed  Google Scholar 

  44. Vetriani, C., Jannasch, H. W., MacGregor, B. J., Stahl, D. A. & Reysenbach, A. L. Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl. Environ. Microbiol. 65, 4375–4384 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Jungbluth, S. P., Amend, J. P. & Rappé, M. S. Metagenome sequencing and 98 microbial genomes from Juan de Fuca Ridge flank subsurface fluids. Sci. Data 4, 170037 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Carr, S. A. et al. Carboxydotrophy potential of uncultivated Hydrothermarchaeota from the subseafloor crustal biosphere. ISME J. 13, 1457–1468 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Chuvochina, M. et al. The importance of designating type material for uncultured taxa. Syst. Appl. Microbiol. 42, 15–21 (2019).

    Article  PubMed  Google Scholar 

  48. Lazar, C. S., Baker, B. J., Seitz, K. W. & Teske, A. P. Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches. ISME J. 11, 1058 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Probst, A. J. et al. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat. Microbiol. 3, 328–336 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Probst, A. J. et al. Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface. Nat. Commun. 5, 5497 (2014).

    Article  CAS  PubMed  Google Scholar 

  51. Teske, A. & Sørensen, K. B. Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J. 2, 3–18 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D. & DeLong, E. F. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484–487 (2001).

    Article  CAS  PubMed  Google Scholar 

  53. Hallam, S. J. et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457–1462 (2004).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  55. Haroon, M. F. et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500, 567–570 (2013).

    Article  CAS  PubMed  Google Scholar 

  56. McGlynn, S. E., Chadwick, G. L., Kempes, C. P. & Orphan, V. J. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526, 531–535 (2015).

    Article  CAS  PubMed  Google Scholar 

  57. Scheller, S., Yu, H., Chadwick, G. L., McGlynn, S. E. & Orphan, V. J. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351, 703–707 (2016).

    Article  CAS  PubMed  Google Scholar 

  58. Laso-Pérez, R. et al. Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature 539, 396–401 (2016).

    Article  PubMed  CAS  Google Scholar 

  59. Lloyd, K. G., Lapham, L. & Teske, A. An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments. Appl. Environ. Microbiol. 72, 7218–7230 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Maignien, L. et al. Anaerobic oxidation of methane in hypersaline cold seep sediments. FEMS Microbiol. Ecol. 83, 214–231 (2013).

    Article  CAS  PubMed  Google Scholar 

  61. Dombrowski, N., Seitz, K. W., Teske, A. P. & Baker, B. J. Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments. Microbiome 5, 106 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Borrel, G. et al. Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. Nat. Microbiol. 4, 603–613 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Chen, S.-C. et al. Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep. Nature 568, 108–111 (2019).

    Article  CAS  PubMed  Google Scholar 

  64. Offre, P., Spang, A. & Schleper, C. Archaea in biogeochemical cycles. Annu. Rev. Microbiol. 67, 437–457 (2013).

    Article  CAS  PubMed  Google Scholar 

  65. Mwirichia, R. et al. Metabolic traits of an uncultured archaeal lineage -MSBL1- from brine pools of the Red Sea. Sci. Rep. 6, 19181 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Takai, K., Moser, D. P., DeFlaun, M., Onstott, T. C. & Fredrickson, J. K. Archaeal diversity in waters from deep South African gold mines. Appl. Environ. Microbiol. 67, 5750–5760 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Inagaki, F. et al. Microbial communities associated with geological horizons in coastal subseafloor sediments from the sea of okhotsk. Appl. Environ. Microbiol. 69, 7224–7235 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Parkes, R. J. et al. Deep sub-seafloor prokaryotes stimulated at interfaces over geological time. Nature 436, 390–394 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Biddle, J. F. et al. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc. Natl Acad. Sci. USA 103, 3846–3851 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Takai, K. & Horikoshi, K. Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152, 1285–1297 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Reysenbach, A.-L. et al. A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442, 444–447 (2006).

    Article  CAS  PubMed  Google Scholar 

  72. Knittel, K., Lösekann, T., Boetius, A., Kort, R. & Amann, R. Diversity and distribution of methanotrophic archaea at cold seeps. Appl. Environ. Microbiol. 71, 467–479 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Lloyd, K. G. et al. Predominant archaea in marine sediments degrade detrital proteins. Nature 496, 215–218 (2013).

    Article  CAS  PubMed  Google Scholar 

  74. Dettling, M. D., Yavitt, J. B., Cadillo-Quiroz, H., Sun, C. & Zinder, S. H. Soil–methanogen interactions in two peatlands (Bog, Fen) in central New York State. Geomicrobiol. J. 24, 247–259 (2007).

    Article  CAS  Google Scholar 

  75. Zhou, Z. et al. Genomic and transcriptomic insights into the ecology and metabolism of benthic archaeal cosmopolitan, Thermoprofundales (MBG-D archaea). ISME J. 13, 885–901 (2019).

    Article  CAS  PubMed  Google Scholar 

  76. Massana, R., DeLong, E. F. & Pedrós-Alió, C. A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl. Environ. Microbiol. 66, 1777–1787 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Fuhrman, J. A. & Davis, A. A. Widespread Archaea and novel Bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar. Ecol. Prog. Ser. 150, 275–285 (1997).

    Article  Google Scholar 

  78. Martin-Cuadrado, A.-B. et al. A new class of marine Euryarchaeota group II from the Mediterranean deep chlorophyll maximum. ISME J. 9, 1619–1634 (2015).

    Article  CAS  PubMed  Google Scholar 

  79. Li, M. et al. Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea. Nat. Commun. 6, 8933 (2015).

    Article  CAS  PubMed  Google Scholar 

  80. Tully, B. J. Metabolic diversity within the globally abundant Marine Group II Euryarchaea offers insight into ecological patterns. Nat. Commun. 10, 271 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Rinke, C. et al. A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.). ISME J. 13, 663–675 (2019).

    Article  CAS  PubMed  Google Scholar 

  82. Orsi, W. D. et al. Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean. ISME J. 10, 2158–2173 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Huber, H. et al. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63–67 (2002).

    Article  CAS  PubMed  Google Scholar 

  84. Waters, E. et al. The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc. Natl Acad. Sci. USA 100, 12984–12988 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Baker, B. J. et al. Lineages of acidophilic archaea revealed by community genomic analysis. Science 314, 1933–1935 (2006).

    Article  CAS  PubMed  Google Scholar 

  86. Baker, B. J. et al. Enigmatic, ultrasmall, uncultivated Archaea. Proc. Natl Acad. Sci. USA 107, 8806–8811 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Narasingarao, P. et al. De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J. 6, 81–93 (2012).

    Article  CAS  PubMed  Google Scholar 

  88. Castelle, C. J. et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 25, 690–701 (2015).

    Article  CAS  PubMed  Google Scholar 

  89. Schwank, K. et al. An archaeal symbiont-host association from the deep terrestrial subsurface. ISME J. 13, 2135–2139 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Parks, D. H. et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat. Microbiol. 2, 1533–1542 (2017).

    Article  CAS  PubMed  Google Scholar 

  91. Bird, J. T., Baker, B. J., Probst, A. J., Podar, M. & Lloyd, K. G. Culture independent genomic comparisons reveal environmental adaptations for Altiarchaeales. Front. Microbiol. 7, 1221 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Krause, S., Bremges, A., Münch, P. C., McHardy, A. C. & Gescher, J. Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms. Sci. Rep. 7, 3289 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Hamm, J. N. et al. Unexpected host dependency of Antarctic Nanohaloarchaeota. Proc. Natl Acad. Sci. USA 116, 14661–14670 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Comolli, L. R., Baker, B. J., Downing, K. H., Siegerist, C. E. & Banfield, J. F. Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon. ISME J. 3, 159–167 (2009).

    Article  CAS  PubMed  Google Scholar 

  95. Heimerl, T. et al. A complex endomembrane system in the Archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Front. Microbiol. 8, 1072 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Burstein, D. et al. New CRISPR–Cas systems from uncultivated microbes. Nature 542, 237–241 (2017).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  98. Spang, A. et al. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 18, 331–340 (2010).

    Article  CAS  PubMed  Google Scholar 

  99. Elkins, J. G. et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl Acad. Sci. USA 105, 8102–8107 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Vanwonterghem, I. et al. Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat. Microbiol. 1, 16170 (2016).

    Article  CAS  PubMed  Google Scholar 

  101. Blöchl, E. et al. Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113 °C. Extremophiles 1, 14–21 (1997).

    Article  PubMed  Google Scholar 

  102. Cubonová, L., Sandman, K., Hallam, S. J., Delong, E. F. & Reeve, J. N. Histones in crenarchaea. J. Bacteriol. 187, 5482–5485 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Brock, T. D., Brock, K. M., Belly, R. T. & Weiss, R. L. Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Archiv. Mikrobiol. 84, 54–68 (1972).

    Article  CAS  Google Scholar 

  104. Zhang, C., Phillips, A. P. R., Wipfler, R. L., Olsen, G. J. & Whitaker, R. J. The essential genome of the crenarchaeal model Sulfolobus islandicus. Nat. Commun. 9, 4908 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Zillig, W. et al. The Archaebacterium Thermofilum pendens represents, a novel genus of the thermophilic, anaerobic sulfur respiring Thermoproteales. Syst. Appl. Microbiol. 4, 79–87 (1983).

    Article  CAS  PubMed  Google Scholar 

  106. Nakagawa, S. Aeropyrum camini sp. nov., a strictly aerobic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney. Int. J. Syst. Evol. Microbiol. 54, 329–335 (2004).

    Article  CAS  PubMed  Google Scholar 

  107. Kozubal, M. A. et al. Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park. ISME J. 7, 622–634 (2013).

    Article  CAS  PubMed  Google Scholar 

  108. Guy, L., Spang, A., Saw, J. H. & Ettema, T. J. G. ‘Geoarchaeote NAG1’ is a deeply rooting lineage of the archaeal order Thermoproteales rather than a new phylum. ISME J. 8, 1353–1357 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  110. Hallam, S. J. et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl Acad. Sci. USA 103, 18296–18301 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Konneke, M. et al. Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation. Proc. Natl Acad. Sci. USA 111, 8239–8244 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  113. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. 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).

    Article  CAS  PubMed  Google Scholar 

  115. 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 

  116. Palatinszky, M. et al. Cyanate as an energy source for nitrifiers. Nature 524, 105–108 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Santoro, A. E., Buchwald, C., McIlvin, M. R. & Casciotti, K. L. Isotopic signature of N2O produced by marine ammonia-oxidizing Archaea. Science 333, 1282–1285 (2011).

    Article  CAS  PubMed  Google Scholar 

  118. Metcalf, W. W. et al. Synthesis of methylphosphonic acid by marine microbes: a source for methane in the aerobic ocean. Science 337, 1104–1107 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Hua, Z.-S. et al. Insights into the ecological roles and evolution of methyl–coenzyme M reductase-containing hot spring Archaea. Nat. Commun. 10, 4574 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  121. Leininger, S. et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809 (2006).

    Article  CAS  PubMed  Google Scholar 

  122. Pachiadaki, M. G., Yakimov, M. M., LaCono, V., Leadbetter, E. & Edgcomb, V. Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin. ISME J. 8, 2478–2489 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Gubry-Rangin, C. et al. Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota. Proc. Natl Acad. Sci. USA 112, 9370–9375 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. de la Torre, J. R., Walker, C. B., Ingalls, A. E., Könneke, M. & Stahl, D. A. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 10, 810–818 (2008).

    Article  PubMed  CAS  Google Scholar 

  125. Durbin, A. M. & Teske, A. Microbial diversity and stratification of South Pacific abyssal marine sediments. Environ. Microbiol. 13, 3219–3234 (2011).

    Article  PubMed  Google Scholar 

  126. Qin, W., Martens-Habbena, W., Kobelt, J. N. & Stahl, D. A. in Bergey’s Manual of Systematics of Archaea and Bacteria (eds Whitman, W. B. et al.) 1–2 (Wiley, 2016).

  127. Stahl, D. A. & de la Torre, J. R. Physiology and diversity of ammonia-oxidizing Archaea. Annu. Rev. Microbiol. 66, 83–101 (2012).

    Article  CAS  PubMed  Google Scholar 

  128. Vajrala, N. et al. Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. Proc. Natl Acad. Sci. USA 110, 1006–1011 (2013).

    Article  CAS  PubMed  Google Scholar 

  129. Stieglmeier, M. et al. Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J. 8, 1135–1146 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Kozlowski, J. A., Stieglmeier, M., Schleper, C., Klotz, M. G. & Stein, L. Y. Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J. 10, 1836–1845 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Liu, S. et al. Abiotic conversion of extracellular NH2OH contributes to N2O emission during ammonia oxidation. Environ. Sci. Technol. 51, 13122–13132 (2017).

    Article  CAS  PubMed  Google Scholar 

  132. Kallmeyer, J., Pockalny, R., Adhikari, R. R., Smith, D. C. & D’Hondt, S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl Acad. Sci. USA 109, 16213–16216 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Kubo, K. et al. Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments. ISME J. 6, 1949–1965 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Meng, J. et al. An uncultivated crenarchaeota contains functional bacteriochlorophyll a synthase. ISME J. 3, 106–116 (2009).

    Article  CAS  PubMed  Google Scholar 

  135. Meng, J. et al. Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J. 8, 650–659 (2014).

    Article  CAS  PubMed  Google Scholar 

  136. Ochsenreiter, T., Selezi, D., Quaiser, A., Bonch-Osmolovskaya, L. & Schleper, C. Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ. Microbiol. 5, 787–797 (2003).

    Article  CAS  PubMed  Google Scholar 

  137. Jurgens, G. Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridization. FEMS Microbiol. Ecol. 34, 45–56 (2000).

    CAS  PubMed  Google Scholar 

  138. McKay, L. J., Hatzenpichler, R., Inskeep, W. P. & Fields, M. W. Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments. Sci. Rep. 7, 7252 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  139. Lazar, C. S. et al. Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ. Microbiol. 18, 1200–1211 (2016).

    Article  CAS  PubMed  Google Scholar 

  140. He, Y. et al. Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat. Microbiol. 1, 16035 (2016).

    Article  CAS  PubMed  Google Scholar 

  141. Meador, T. B. et al. The archaeal lipidome in estuarine sediment dominated by members of the Miscellaneous Crenarchaeotal Group. Environ. Microbiol. 17, 2441–2458 (2015).

    Article  CAS  PubMed  Google Scholar 

  142. Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).

    Article  CAS  PubMed  Google Scholar 

  143. Yu, T. et al. Growth of sedimentary Bathyarchaeota on lignin as an energy source. Proc. Natl Acad. Sci. USA 115, 6022–6027 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. McKay, L. J. et al. Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota. Nat. Microbiol. 4, 614–622 (2019).

    Article  CAS  PubMed  Google Scholar 

  145. Nunoura, T. et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39, 3204–3223 (2011).

    Article  CAS  PubMed  Google Scholar 

  146. Beam, J. P. et al. Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community. ISME J. 10, 210–224 (2016).

    Article  CAS  PubMed  Google Scholar 

  147. Gaiman, N. Norse Mythology (Bloomsbury Publishing, 2017).

  148. 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 

  149. Akıl, C. & Robinson, R. C. Genomes of Asgard archaea encode profilins that regulate actin. Nature 562, 439–443 (2018).

    Article  PubMed  CAS  Google Scholar 

  150. Seitz, K. W., Lazar, C. S., Hinrichs, K.-U., Teske, A. P. & Baker, B. J. Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J. 10, 1696–1705 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).

    Article  CAS  PubMed  Google Scholar 

  152. Seitz, K. W. et al. Asgard archaea capable of anaerobic hydrocarbon cycling. Nat. Commun. 10, 1822 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  153. Hochstrasser, M. Origin and function of ubiquitin-like proteins. Nature 458, 422–429 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Hurley, J. H. ESCRTs are everywhere. EMBO J. 34, 2398–2407 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Ettema, T. J. G., Lindås, A.-C. & Bernander, R. An actin-based cytoskeleton in archaea. Mol. Microbiol. 80, 1052–1061 (2011).

    Article  CAS  PubMed  Google Scholar 

  156. Koonin, E. V. & Yutin, N. The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb. Persp. Biol. 6, a016188 (2014).

    Article  CAS  Google Scholar 

  157. Dalziel, M., Crispin, M., Scanlan, C. N., Zitzmann, N. & Dwek, R. A. Emerging principles for the therapeutic exploitation of glycosylation. Science 343, 1235681 (2014).

    Article  PubMed  CAS  Google Scholar 

  158. Koga, Y., Kyuragi, T., Nishihara, M. & Sone, N. Did archaeal and bacterial cells arise independently from noncellular precursors? A hypothesis stating that the advent of membrane phospholipid with enantiomeric glycerophosphate backbones caused the separation of the two lines of descent. J. Mol. Evol. 47, 631–631 (1998).

    Article  CAS  PubMed  Google Scholar 

  159. Sojo, V., Pomiankowski, A. & Lane, N. A bioenergetic basis for membrane divergence in archaea and bacteria. PLoS Biol. 12, e1001926 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  160. Gray, M. W. & Doolittle, W. F. Has the endosymbiont hypothesis been proven? Microbiol. Rev. 46, 1–42 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Villanueva, L., Schouten, S. & Sinninghe Damsté, J. S. Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the ‘lipid divide’. Environ. Microbiol. 19, 54–69 (2017).

    Article  CAS  PubMed  Google Scholar 

  162. Spang, A. et al. Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism. Nat. Microbiol. 4, 1138–1148 (2019).

    Article  CAS  PubMed  Google Scholar 

  163. Imachi, H. et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature 577, 519–525 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).

    Article  CAS  PubMed  Google Scholar 

  165. Bird, J. T. et al. Uncultured microbial phyla suggest mechanisms for multi-thousand-year subsistence in Baltic Sea sediments. mBio 10, e02376–18 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Nielsen, J. L. & Nielsen, P. H. in Handbook of Hydrocarbon and Lipid Microbiology (ed. Timmis, K. N.) 4093–4102 (2010).

  167. Hatzenpichler, R. et al. Visualizing in situ translational activity for identifying and sorting slow-growing archaeal-bacterial consortia. Proc. Natl Acad. Sci. USA 113, E4069–E4078 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Michalska, K. et al. New aminopeptidase from ‘microbial dark matter’ archaeon. FASEB J. 29, 4071–4079 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Martijn, J. & Ettema, T. J. G. From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem. Soc. Trans. 41, 451–457 (2013).

    Article  CAS  PubMed  Google Scholar 

  170. Jay, Z. J. et al. Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats. Nat. Microbiol. 3, 732–740 (2018).

    Article  CAS  PubMed  Google Scholar 

  171. Nurk, S., Meleshko, D., Korobeynikov, A. & Pevzner, P. A. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 27, 824–834 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Alneberg, J. et al. Binning metagenomic contigs by coverage and composition. Nat. Methods 11, 1144–1146 (2014).

    Article  CAS  PubMed  Google Scholar 

  173. Eren, A. M. et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3, e1319 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  174. Kang, D. D., Froula, J., Egan, R. & Wang, Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3, e1165 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  175. Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Pace, N. R. Mapping the tree of life: progress and prospects. Microbiol. Mol. Biol. Rev. 73, 565–576 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Baker, B. J., Lazar, C. S., Teske, A. P. & Dick, G. J. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome 3, 14 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  178. Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523, 208–211 (2015).

    Article  CAS  PubMed  Google Scholar 

  179. Sorek, R. et al. Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318, 1449–1452 (2007).

    Article  CAS  PubMed  Google Scholar 

  180. Petitjean, C., Deschamps, P., López-García, P. & Moreira, D. Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol. Evol. 7, 191–204 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  181. Williams, T. A. et al. Integrative modeling of gene and genome evolution roots the archaeal tree of life. Proc. Natl Acad. Sci. USA 114, E4602–E4611 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  182. Toft, C. & Andersson, S. G. E. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat. Rev. Genet. 11, 465–475 (2010).

    Article  CAS  PubMed  Google Scholar 

  183. Das, S., Paul, S., Bag, S. K. & Dutta, C. Analysis of Nanoarchaeum equitans genome and proteome composition: indications for hyperthermophilic and parasitic adaptation. BMC Genomics 7, 186 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  184. Podar, M. et al. A genomic analysis of the archaeal system Ignicoccus hospitalisNanoarchaeum equitans. Genome Biol. 9, R158 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  185. Hua, Z.-S. et al. Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota. Nat. Commun. 9, 2832 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  186. Adam, P. S., Borrel, G. & Gribaldo, S. An archaeal origin of the Wood–Ljungdahl HMPT branch and the emergence of bacterial methylotrophy. Nat. Microbiol. 4, 2155–2163 (2019).

    Article  PubMed  CAS  Google Scholar 

  187. Borrel, G., Adam, P. S. & Gribaldo, S. Methanogenesis and the Wood–Ljungdahl pathway: an ancient, versatile, and fragile association. Genome Biol. Evol. 8, 1706–1711 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Chistoserdova, L. The enigmatic planctomycetes may hold a key to the origins of methanogenesis and methylotrophy. Mol. Biol. Evol. 21, 1234–1241 (2004).

    Article  CAS  PubMed  Google Scholar 

  189. Chistoserdova, L. Wide distribution of genes for tetrahydromethanopterin/methanofuran-linked C1 transfer reactions argues for their presence in the common ancestor of bacteria and archaea. Front. Microbiol. 7, 1425 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  190. Ueno, Y., Yamada, K., Yoshida, N., Maruyama, S. & Isozaki, Y. Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era. Nature 440, 516–519 (2006).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This review was supported by the National Science Foundation Systematics and Biodiversity Sciences award no. 1737298 (to B.J.B.), grant no. NSF-OCE-1431598 (to K.G.L.) and the Simons Foundation grant no. 404586 (to K.G.L.).

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B.J.B. and A.E.S. wrote this review and all authors provided input. B.J.B., K.W.S. and V.D.A. generated the phylogeny. B.J.B., K.G.L., V.D.A. and N.D. generated the figures.

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Correspondence to Brett J. Baker.

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List of genomes included in analyses in Figs. 1 and 4.

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Baker, B.J., De Anda, V., Seitz, K.W. et al. Diversity, ecology and evolution of Archaea. Nat Microbiol 5, 887–900 (2020). https://doi.org/10.1038/s41564-020-0715-z

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