Phylogenomics suggests oxygen availability as a driving force in Thaumarchaeota evolution


Ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread in marine and terrestrial habitats, playing a major role in the global nitrogen cycle. However, their evolutionary history remains unexplored, which limits our understanding of their adaptation mechanisms. Here, our comprehensive phylogenomic tree of Thaumarchaeota supports three sequential events: origin of AOA from terrestrial non-AOA ancestors, colonization of the shallow ocean, and expansion to the deep ocean. Careful molecular dating suggests that these events coincided with the Great Oxygenation Event around 2300 million years ago (Mya), and oxygenation of the shallow and deep ocean around 800 and 635–560 Mya, respectively. The first transition was likely enabled by the gain of an aerobic pathway for energy production by ammonia oxidation and biosynthetic pathways for cobalamin and biotin that act as cofactors in aerobic metabolism. The first transition was also accompanied by the loss of dissimilatory nitrate and sulfate reduction, loss of oxygen-sensitive pyruvate oxidoreductase, which reduces pyruvate to acetyl-CoA, and loss of the Wood–Ljungdahl pathway for anaerobic carbon fixation. The second transition involved gain of a K+ transporter and of the biosynthetic pathway for ectoine, which may function as an osmoprotectant. The third transition was accompanied by the loss of the uvr system for repairing ultraviolet light-induced DNA lesions. We conclude that oxygen availability drove the terrestrial origin of AOA and their expansion to the photic and dark oceans, and that the stressors encountered during these events were partially overcome by gene acquisitions from Euryarchaeota and Bacteria, among other sources.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1
Fig. 2


  1. 1.

    Karner MB, DeLong EF, Karl DM. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature. 2001;409:507–10.

  2. 2.

    Teira E, Lebaron P, van Aken H, Herndl GJ. Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic. Limnol Oceanogr. 2006;51:2131–44.

  3. 3.

    Buckley DH, Graber JR, Schmidt TM. Phylogenetic analysis of nonthermophilic members of the kingdom Crenarchaeota and their diversity and abundance in soils. Appl Environ Microbiol. 1998;64:4333–9.

  4. 4.

    Torsten O, Drazenka S, Achim Q, Liza B-O, Christa S. Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol. 2003;5:787–97.

  5. 5.

    Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. Ubiquity and diversity of ammonia-oxidizing Archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA. 2005;102:14683–8.

  6. 6.

    Stahl DA, de la Torre JR. Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol. 2012;66:83–101.

  7. 7.

    Stieglmeier M, Alves RJE, Schleper C. The Phylum Thaumarchaeota. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The prokaryotes: other major lineages of bacteria and the Archaea. Berlin Heidelberg: Springer; 2014. p. 347–62.

  8. 8.

    Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P, et al. Archaeal nitrification in the ocean. Proc Natl Acad Sci USA. 2006;103:12317–22.

  9. 9.

    Nicol GW, Leininger S, Schleper C. Distribution and activity of ammonia-oxidizing Archaea in natural environments. In: Ward BB, Arp DJ, Klotz MJ, editors. Nitrification. Washington, DC: ASM Press; 2011. p. 157−78.

  10. 10.

    Groussin M, Gouy M. Adaptation to environmental temperature is a major determinant of molecular evolutionary rates in Archaea. Mol Biol Evol. 2011;28:2661–74.

  11. 11.

    Alves RJE, Minh BQ, Urich T, von Haeseler A, Schleper C. Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat Commun. 2018;9:1517.

  12. 12.

    Abby SS, Melcher M, Kerou M, Krupovic M, Stieglmeier M, Rossel C, et al. Candidatus Nitrosocaldus cavascurensis, an ammonia oxidizing, extremely thermophilic archaeon with a highly mobile genome. Front Microbiol. 2018;9:28.

  13. 13.

    Brochier-Armanet C, Gribaldo S, Forterre P. Spotlight on the Thaumarchaeota. ISME J. 2012;6:227–30.

  14. 14.

    Daebeler A, Herbold CW, Vierheilig J, Sedlacek CJ, Pjevac P, Albertsen M, et al. Cultivation and genomic analysis of “Candidatus Nitrosocaldus islandicus,” an obligately thermophilic, ammonia-oxidizing thaumarchaeon from a hot spring biofilm in Graendalur Valley, Iceland. Front Microbiol. 2018;9:193.

  15. 15.

    Lopez-Garcia P, Zivanovic Y, Deschamps P, Moreira D. Bacterial gene import and mesophilic adaptation in archaea. Nat Rev Microbiol. 2015;13:447–56.

  16. 16.

    López-García P, Brochier C, Moreira D, Rodríguez-Valera F. Comparative analysis of a genome fragment of an uncultivated mesopelagic crenarchaeote reveals multiple horizontal gene transfers. Environ Microbiol. 2004;6:19–34.

  17. 17.

    Deschamps P, Zivanovic Y, Moreira D, Rodriguez-Valera F, Lopez-Garcia P. Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic thaumarchaeota and euryarchaeota. Genome Biol Evol. 2014;6:1549–63.

  18. 18.

    Hua Z-S, Qu Y-N, Zhu Q, Zhou E-M, Qi Y-L, Yin Y-R, et al. Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota. Nat Commun. 2018;9:2832.

  19. 19.

    Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng J-F, et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature. 2013;499:431–7.

  20. 20.

    Beam JP, Jay ZJ, Kozubal MA, Inskeep WP. Niche specialization of novel Thaumarchaeota to oxic and hypoxic acidic geothermal springs of Yellowstone National Park. ISME J. 2014;8:938–51.

  21. 21.

    Lin X, Handley KM, Gilbert JA, Kostka JE. Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat. ISME J. 2015;9:2740–4.

  22. 22.

    Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun. 2016;7:13219.

  23. 23.

    Weber EB, Lehtovirta-Morley LE, Prosser JI, Gubry-Rangin C. Ammonia oxidation is not required for growth of Group 1.1c soil Thaumarchaeota. FEMS Microbiol Ecol. 2015;91:fiv001.

  24. 24.

    Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74.

  25. 25.

    Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D, Reddy TBK, et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol. 2017;35:725.

  26. 26.

    Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586–91.

  27. 27.

    Blank CE. An expansion of age constraints for microbial clades that lack a conventional fossil record using phylogenomic dating. J Mol Evol. 2011;73:188–208.

  28. 28.

    Wolfe JM, Fournier GP. Horizontal gene transfer constrains the timing of methanogen evolution. Nat Ecol Evol. 2018;2:897–903.

  29. 29.

    Blank CE. Phylogenomic dating—a method of constraining the age of microbial taxa that lack a conventional fossil record. Astrobiology. 2009;9:173–91.

  30. 30.

    Adam PS, Borrel G, Brochier-Armanet C, Gribaldo S. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J. 2017;11:2407.

  31. 31.

    Petitjean C, Deschamps P, Lopez-Garcia P, Moreira D. Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol Evol. 2014;7:191–204.

  32. 32.

    Raymann K, Brochier-Armanet C, Gribaldo S. The two-domain tree of life is linked to a new root for the Archaea. Proc Natl Acad Sci USA. 2015;112:6670–5.

  33. 33.

    Williams TA, Szöllősi GJ, Spang A, Foster PG, Heaps SE, Boussau B, et al. Integrative modeling of gene and genome evolution roots the archaeal tree of life. Proc Natl Acad Sci USA. 2017;114:E4602–11.

  34. 34.

    Brochier-Armanet C, Deschamps P, Lopez-Garcia P, Zivanovic Y, Rodriguez-Valera F, Moreira D. Complete-fosmid and fosmid-end sequences reveal frequent horizontal gene transfers in marine uncultured planktonic archaea. ISME J. 2011;5:1291–302.

  35. 35.

    Makarova KS, Wolf YI, Koonin EV. Archaeal Clusters of Orthologous Genes (arCOGs): An update and application for analysis of shared features between Thermococcales, Methanococcales, and Methanobacteriales. Life. 2015;5:818–40.

  36. 36.

    Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA. 2010;107:8818–23.

  37. 37.

    Carini P, Dupont Christopher L, Santoro Alyson E. Patterns of thaumarchaeal gene expression in culture and diverse marine environments. Environ Microbiol. 2018;20:2112–24.

  38. 38.

    Santoro AE, Dupont CL, Richter RA, Craig MT, Carini P, McIlvin MR, et al. Genomic and proteomic characterization of “Candidatus Nitrosopelagicus brevis”: an ammonia-oxidizing archaeon from the open ocean. Proc Natl Acad Sci USA. 2015;112:1173–8.

  39. 39.

    Haroon MF, Thompson LR, Parks DH, Hugenholtz P, Stingl U. A catalogue of 136 microbial draft genomes from Red Sea metagenomes. Sci Data. 2016;3:160050.

  40. 40.

    Luo G, Ono S, Beukes NJ, Wang DT, Xie S, Summons RE. Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago. Sci Adv. 2016;2:e1600134.

  41. 41.

    Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, et al. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci USA. 2008;105:2134–9.

  42. 42.

    Jung MY, Kim JG, Sinninghe Damste JS, Rijpstra WI, Madsen EL, Kim SJ, et al. A hydrophobic ammonia-oxidizing archaeon of the Nitrosocosmicus clade isolated from coal tar-contaminated sediment. Environ Microbiol Rep. 2016;8:983–92.

  43. 43.

    Qin W, Meinhardt KA, Moffett JW, Devol AH, Virginia Armbrust E, Ingalls AE, et al. Influence of oxygen availability on the activities of ammonia-oxidizing archaea. Environ Microbiol Rep. 2017b;9:250–6.

  44. 44.

    Bayer B, Vojvoda J, Offre P, Alves RJ, Elisabeth NH, Garcia JA, et al. Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation. ISME J. 2016;10:1051–63.

  45. 45.

    Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA. 2011;108:8420–5.

  46. 46.

    Zhalnina KV, Dias R, Leonard MT, Dorr de Quadros P, Camargo FAO, Drew JC, et al. Genome sequence of Candidatus Nitrososphaera evergladensis from Group I.1b enriched from Everglades soil reveals novel genomic features of the ammonia-oxidizing archaea. PLoS ONE. 2014;9:e101648.

  47. 47.

    Betts HC, Puttick MN, Clark JW, Williams TA, Donoghue PCJ, Pisani D. Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin. Nat Ecol Evol. 2018;2:1556–62.

  48. 48.

    Parham JF, Donoghue PCJ, Bell CJ, Calway TD, Head JJ, Holroyd PA, et al. Best practices for justifying fossil calibrations. Syst Biol. 2012;61:346–59.

  49. 49.

    Schenk JJ. Consequences of secondary calibrations on divergence time estimates. PLoS ONE. 2016;11:e0148228.

  50. 50.

    Blank CE. Not so old Archaea—the antiquity of biogeochemical processes in the archaeal domain of life. Geobiology. 2009;7:495–514.

  51. 51.

    Vajrala N, Martens-Habbena W, Sayavedra-Soto LA, Schauer A, Bottomley PJ, Stahl DA, et al. Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. Proc Natl Acad Sci USA. 2013;110:1006–11.

  52. 52.

    Spang A, Poehlein A, Offre P, Zumbragel S, Haider S, Rychlik N, et al. The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol. 2012;14:3122–45.

  53. 53.

    Spaans S, Weusthuis R, Van Der Oost J, Kengen S. NADPH-generating systems in bacteria and archaea. Front Microbiol. 2015;6:742.

  54. 54.

    Aliverti A, Pandini V, Pennati A, de Rosa M, Zanetti G. Structural and functional diversity of ferredoxin-NADP+ reductases. Arch Biochem Biophys. 2008;474:283–91.

  55. 55.

    Giró M, Carrillo N, Krapp AR. Glucose-6-phosphate dehydrogenase and ferredoxin-NADP(H) reductase contribute to damage repair during the soxRS response of Escherichia coli. Microbiology. 2006;152:1119–28.

  56. 56.

    Heal KR, Qin W, Ribalet F, Bertagnolli AD, Coyote-Maestas W, Hmelo LR, et al. Two distinct pools of B12 analogs reveal community interdependencies in the ocean. Proc Natl Acad Sci USA. 2017;114:364–9.

  57. 57.

    Qin W, Heal KR, Ramdasi R, Kobelt JN, Martens-Habbena W, Bertagnolli AD. et al. Nitrosopumilus maritimus gen. nov., sp. nov., Nitrosopumilus cobalaminigenes sp. nov., Nitrosopumilus oxyclinae sp. nov., and Nitrosopumilus ureiphilus sp. nov., four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota. Int J Syst Evol Microbiol. 2017;67:5067–79.

  58. 58.

    Chow J, Danso D, Ferrer M, Streit WR. The Thaumarchaeon N. gargensis carries functional bioABD genes and has a promiscuous E. coli ΔbioH-complementing esterase EstN1. Sci Rep. 2018;8:13823.

  59. 59.

    Patton DA, Volrath S, Ward ER. Complementation of an Arabidopsis thaliana biotin auxotroph with an Escherichia coli biotin biosynthetic gene. Mol Gen Genet. 1996;251:261–6.

  60. 60.

    Satiaputra J, Shearwin KE, Booker GW, Polyak SW. Mechanisms of biotin-regulated gene expression in microbes. Synth Syst Biotechnol. 2016;1:17–24.

  61. 61.

    Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS. Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem. 2003;278:41148–59.

  62. 62.

    Ishii M, Miyake T, Satoh T, Sugiyama H, Oshima Y, Kodama T, et al. Autotrophic carbon dioxide fixation in Acidianus brierleyi. Arch Microbiol. 1996;166:368–71.

  63. 63.

    Konneke M, Schubert DM, Brown PC, Hugler M, Standfest S, Schwander T, et al. Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation. Proc Natl Acad Sci USA. 2014;111:8239–44.

  64. 64.

    Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes DS, Bonnefoy V. Extending the models for iron and sulfur oxidation in the extreme Acidophile Acidithiobacillus ferrooxidans. BMC Genom. 2009;10:394.

  65. 65.

    Chabrière E, Charon MH, Volbeda A, Pieulle L, Hatchikian EC, Fontecilla–Camps JC. Crystal structures of the key anaerobic enzyme pyruvate:ferredoxin oxidoreductase, free and in complex with pyruvate. Nat Struct Biol. 1999;6:182.

  66. 66.

    Jünemann S. Cytochrome bd terminal oxidase. Biochim Biophys Acta Bioenerg. 1997;1321:107–27.

  67. 67.

    Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science. 2015;350:434–8.

  68. 68.

    Zhou Z, Pan J, Wang F, Gu J, Li M. Bathyarchaeota: globally distributed metabolic generalists in anoxic environments. FEMS Microbiol Rev. 2018;42:639–55.

  69. 69.

    Petitjean C, Moreira D, López-García P, Brochier-Armanet C. Horizontal gene transfer of a chloroplast DnaJ-Fer protein to Thaumarchaeota and the evolutionary history of the DnaK chaperone system in Archaea. BMC Evol Biol. 2012;12:226.

  70. 70.

    Holland HD. The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B Biol Sci. 2006;361:903–15.

  71. 71.

    Planavsky NJ, Reinhard CT, Wang X, Thomson D, McGoldrick P, Rainbird RH, et al. Low Mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals. Science. 2014;346:635–8.

  72. 72.

    Rosen BP. Recent advances in bacterial ion transport. Annu Rev Microbiol. 1986;40:263–86.

  73. 73.

    Sleator RD, Hill C. Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev. 2002;26:49–71.

  74. 74.

    Sahoo SK, Planavsky NJ, Jiang G, Kendall B, Owens JD, Wang X, et al. Oceanic oxygenation events in the anoxic Ediacaran ocean. Geobiology. 2016;14:457–68.

  75. 75.

    Swan BK, Chaffin MD, Martinez-Garcia M, Morrison HG, Field EK, Poulton NJ, et al. Genomic and metabolic diversity of marine group I Thaumarchaeota in the mesopelagic of two subtropical gyres. PLoS ONE. 2014;9:e95380.

  76. 76.

    Luo H, Zhang H, Long RA, Benner R. Depth distributions of alkaline phosphatase and phosphonate utilization genes in the North Pacific Subtropical Gyre. Aquat Microb Ecol. 2011;62:61–9.

  77. 77.

    Luo H, Tolar BB, Swan BK, Zhang CL, Stepanauskas R, Ann Moran M, et al. Single-cell genomics shedding light on marine Thaumarchaeota diversification. ISME J. 2014;8:732–6.

  78. 78.

    Makarova KS, Sorokin AV, Novichkov PS, Wolf YI, Koonin EV. Clusters of orthologous genes for 41 archaeal genomes and implications for evolutionary genomics of archaea. Biol Direct. 2007;2:33.

  79. 79.

    Wolf YI, Makarova KS, Yutin N, Koonin EV. Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol Direct. 2012;7:46.

  80. 80.

    Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3.

  81. 81.

    Khan AU, Mei YH, Wilson T. A proposed function for spermine and spermidine: protection of replicating DNA against damage by singlet oxygen. Proc Natl Acad Sci USA. 1992;89:11426–7.

  82. 82.

    Martinez A, Kolter R. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol. 1997;179:5188–94.

  83. 83.

    Arnold AR, Barton JK. DNA protection by the bacterial ferritin Dps via DNA charge transport. J Am Chem Soc. 2013;135:15726–9.

  84. 84.

    Zeth K. Dps biomineralizing proteins: multifunctional architects of nature. Biochem J. 2012;445:297–311.

  85. 85.

    Gurmu D, Lu J, Johnson KA, Nordlund P, Holmgren A, Erlandsen H. The crystal structure of the protein YhaK from Escherichia coli reveals a new subclass of redox sensitive enterobacterial bicupins. Proteins. 2009;74:18–31.

  86. 86.

    Czech L, Hermann L, Stöveken N, Richter A, Höppner A, Smits S, et al. Role of the extremolytes Ectoine and Hydroxyectoine as stress protectants and nutrients: genetics, phylogenomics, biochemistry, and structural analysis. Genes. 2018;9:177.

  87. 87.

    Widderich N, Czech L, Elling FJ, Konneke M, Stoveken N, Pittelkow M, et al. Strangers in the archaeal world: osmostress-responsive biosynthesis of ectoine and hydroxyectoine by the marine thaumarchaeon Nitrosopumilus maritimus. Environ Microbiol. 2016;18:1227–48.

  88. 88.

    Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y, Sugahara J, et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci USA. 2006;103:18296–301.

  89. 89.

    Ahlgren NA, Chen Y, Needham DM, Parada AE, Sachdeva R, Trinh V, et al. Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification and multiple restriction systems. Environ Microbiol. 2017;19:2434–52.

  90. 90.

    Young JC. Mechanisms of the Hsp70 chaperone system. Biochem Cell Biol. 2010;88:291–300.

  91. 91.

    Plominsky AM, Trefault N, Podell S, Blanton JM, De la Iglesia R, Allen EE, et al. Metabolic potential and in situ transcriptomic profiles of previously uncharacterized key microbial groups involved in coupled carbon, nitrogen and sulfur cycling in anoxic marine zones. Environ Microbiol. 2018;20:2727–42.

  92. 92.

    Beam JP, Jay ZJ, Schmid MC, Rusch DB, Romine MF, Jennings Rd M, et al. Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community. ISME J. 2015;10:210.

  93. 93.

    He Y, Li M, Perumal V, Feng X, Fang J, Xie J, et al. Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol. 2016;1:16035.

  94. 94.

    Lazar CS, Baker BJ, Seitz K, Hyde AS, Dick GJ, Hinrichs KU, et al. Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ Microbiol. 2016;18:1200–11.

  95. 95.

    Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, et al. Predominant archaea in marine sediments degrade detrital proteins. Nature. 2013;496:215–8.

  96. 96.

    Somero GN, Lockwood B, Tomanek L. Oxygen and metabolism. In: Somero GN, Lockwood B, Tomanek L, editors. Biochemical adaptation. Massachusetts: Sinauer Associates, Inc. Publishers; 2017.

Download references


We thank Professor Chuanlun Zhang and Professor Mary Ann Moran for their comments in the earlier versions of the manuscript. This research is supported by the National Key R&D Program of China (2018YFC0309800), the National Science Foundation of China (41776129), and the Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M-403/16). Work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported under Contract No. DE-AC02-05CH11231. JTH’s participation was supported by NSF OCE 15-38677. We thank three anonymous reviewers for their useful comments. The views and conclusions contained in this document are those of the authors and should not be interpreted as necessarily representing the official policies, either expressed or implied, of the DHS or S&T. In no event shall DHS, NBACC, S&T or Battelle National Biodefense Institute have any responsibility or liability for any use, misuse, inability to use, or reliance upon the information contained herein. DHS does not endorse any products or commercial services mentioned in this publication.

Author information

Correspondence to Haiwei Luo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ren, M., Feng, X., Huang, Y. et al. Phylogenomics suggests oxygen availability as a driving force in Thaumarchaeota evolution. ISME J 13, 2150–2161 (2019).

Download citation

Further reading