1932

Abstract

Archaea are ubiquitous and abundant members of the marine plankton. Once thought of as rare organisms found in exotic extremes of temperature, pressure, or salinity, archaea are now known in nearly every marine environment. Though frequently referred to collectively, the planktonic archaea actually comprise four major phylogenetic groups, each with its own distinct physiology and ecology. Only one group—the marine Thaumarchaeota—has cultivated representatives, making marine archaea an attractive focus point for the latest developments in cultivation-independent molecular methods. Here, we review the ecology, physiology, and biogeochemical impact of the four archaeal groups using recent insights from cultures and large-scale environmental sequencing studies. We highlight key gaps in our knowledge about the ecological roles of marine archaea in carbon flow and food web interactions. We emphasize the incredible uncultivated diversity within each of the four groups, suggesting there is much more to be done.

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2019-01-03
2024-06-14
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Literature Cited

  1. Adam PS, Borrel G, Brochier-Armanet C, Gribaldo S 2017. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J 11:2407–25
    [Google Scholar]
  2. Agogue H, Brink M, Dinasquet J, Herndl GJ 2008. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456:788–91
    [Google Scholar]
  3. Ahlgren NA, Chen Y, Needham DM, Parada AE, Sachdeva R et al. 2017. Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification and multiple restriction systems. Environ. Microbiol. 19:2434–52
    [Google Scholar]
  4. Alonso-Saez L, Waller AS, Mende DR, Bakker K, Farnelid H et al. 2012. Role for urea in nitrification by polar marine Archaea. PNAS 109:17989–94
    [Google Scholar]
  5. Alves RJE, Minh BQ, Urich T, von Haeseler A, Schleper C 2018. Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat. Commun. 9:1517
    [Google Scholar]
  6. Amin SA, Moffett JW, Martens-Habbena W, Jacquot JE, Han Y et al. 2013. Copper requirements of the ammonia-oxidizing archaeon Nitrosopumilus maritimus SCM1 and implications for nitrification in the marine environment. Limnol. Oceanogr. 58:2037–45
    [Google Scholar]
  7. Anderson R, Winter C, Jürgens K 2012. Protist grazing and viral lysis as prokaryotic mortality factors at Baltic Sea oxic–anoxic interfaces. Mar. Ecol. Prog. Ser. 467:1–14
    [Google Scholar]
  8. Arp DJ, Sayavedra-Soto LA, Hommes NG 2002. Molecular biology and biochemistry of ammonia oxidation by Nitrosomonas europaea. Arch. Microbiol 178:250–55
    [Google Scholar]
  9. Baker BJ, Lesniewski RA, Dick GJ 2012. Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume. ISME J 6:2269–79
    [Google Scholar]
  10. Baker BJ, Sheik CS, Taylor CA, Jain S, Bhasi A et al. 2013. Community transcriptomic assembly reveals microbes that contribute to deep-sea carbon and nitrogen cycling. ISME J 7:1962–73
    [Google Scholar]
  11. Bano N, Ruffin S, Ransom B, Hollibaugh JT 2004. Phylogenetic composition of Arctic Ocean archaeal assemblages and comparison with Antarctic assemblages. Appl. Environ. Microbiol. 70:781–89
    [Google Scholar]
  12. Bayer B, Vojvoda J, Offre P, Alves RJE, Elisabeth NH et al. 2015. Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation. ISME J 10:1051–63
    [Google Scholar]
  13. Béjà O, Suzuki MT, Koonin EV, Aravind L, Hadd A et al. 2000. Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environ. Microbiol. 2:516–29
    [Google Scholar]
  14. Belmar L, Molina V, Ulloa O 2011. Abundance and phylogenetic identity of archaeoplankton in the permanent oxygen minimum zone of the eastern tropical South Pacific. FEMS Microbiol. Ecol. 78:314–26
    [Google Scholar]
  15. Beman JM, Chow CE, King AL, Feng YY, Fuhrman JA et al. 2011.a Global declines in oceanic nitrification rates as a consequence of ocean acidification. PNAS 108:208–13
    [Google Scholar]
  16. Beman JM, Popp BN, Francis CA 2008. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2:429–41
    [Google Scholar]
  17. Beman JM, Sachdeva R, Fuhrman JA 2010. Population ecology of nitrifying Archaea and Bacteria in the Southern California Bight. Environ. Microbiol. 12:1282–92
    [Google Scholar]
  18. Beman JM, Steele JA, Fuhrman JA 2011.b Co-occurrence patterns for abundant marine archaeal and bacterial lineages in the deep chlorophyll maximum of coastal California. ISME J 5:1077–85
    [Google Scholar]
  19. Berg C, Listmann L, Vandieken V, Vogts A, Jürgens K 2015.a Chemoautotrophic growth of ammonia-oxidizing Thaumarchaeota enriched from a pelagic redox gradient in the Baltic Sea. Front. Microbiol. 5:786
    [Google Scholar]
  20. Berg C, Vandieken V, Thamdrup B, Jürgens K 2015.b Significance of archaeal nitrification in hypoxic waters of the Baltic Sea. ISME J 9:1319–32
    [Google Scholar]
  21. Berg IA, Kockelkorn D, Buckel W, Fuchs G 2007. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea. Science 318:1782–86
    [Google Scholar]
  22. Bergauer K, Fernandez-Guerra A, Garcia JAL, Sprenger RR, Stepanauskas R et al. 2018. Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics. PNAS 115:E400–8
    [Google Scholar]
  23. Biller SJ, Mosier AC, Wells GF, Francis CA 2012. Global biodiversity of aquatic ammonia-oxidizing archaea is partitioned by habitat. Front. Microbiol. 3:252
    [Google Scholar]
  24. Boutrif M, Garel M, Cottrell MT, Tamburini C 2011. Assimilation of marine extracellular polymeric substances by deep-sea prokaryotes in the NW Mediterranean Sea. Environ. Microbiol. Rep. 3:705–9
    [Google Scholar]
  25. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P 2008. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6:245–52
    [Google Scholar]
  26. Buchwald C, Santoro AE, Stanley RH, Casciotti KL 2015. Nitrogen cycling in the secondary nitrite maximum of the eastern tropical North Pacific off Costa Rica. Glob. Biogeochem. Cycles 29:2061–81
    [Google Scholar]
  27. Caranto JD, Lancaster KM 2017. Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase. PNAS 114:8217–22
    [Google Scholar]
  28. Carini P, Dupont CL, Santoro AE 2018. Patterns of thaumarchaeal gene expression in culture and diverse marine environments. Environ. Microbiol. 20:2112–24
    [Google Scholar]
  29. Chow CET, Winget DM, White RA, Hallam SJ, Suttle CA 2015. Combining genomic sequencing methods to explore viral diversity and reveal potential virus-host interactions. Front. Microbiol. 6:265
    [Google Scholar]
  30. Church MJ, Karl DM, DeLong EF 2010. Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean. Environ. Microbiol. 12:679–88
    [Google Scholar]
  31. Crump BC, Baross JA 2000. Archaeaplankton in the Columbia River, its estuary and the adjacent coastal ocean, USA. FEMS Microbiol. Ecol. 31:231–39
    [Google Scholar]
  32. Damashek J, Pettie KP, Brown ZW, Mills MM, Arrigo KR, Francis CA 2017. Regional patterns in ammonia-oxidizing communities throughout Chukchi Sea waters from the Bering Strait to the Beaufort Sea. Aquat. Microb. Ecol. 79:273–86
    [Google Scholar]
  33. Danovaro R, Rastelli E, Corinaldesi C, Tangherlini M, Dell'Anno A 2017. Marine archaea and archaeal viruses under global change. F1000Research 6:1241
    [Google Scholar]
  34. DeLong EF 1992. Archaea in coastal marine environments. PNAS 89:5685–89
    [Google Scholar]
  35. DeLong EF 2007. Microbial domains in the ocean: a lesson from the Archaea. Oceanography 20:2124–29
    [Google Scholar]
  36. DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ et al. 2006. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311:496–503
    [Google Scholar]
  37. DeLong EF, Taylor LT, Marsh TL, Preston CM 1999. Visualization and enumeration of marine planktonic archaea and bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl. Environ. Microbiol. 65:5554–63
    [Google Scholar]
  38. DeLong EF, Wu KY, Prezelin BB, Jovine RVM 1994. High abundance of Archaea in Antarctic marine picoplankton. Nature 371:695–97
    [Google Scholar]
  39. Deschamps P, Zivanovic Y, Moreira D, Rodríguez-Valera F, López-Garcia P 2014. Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic Thaumarchaeota and Euryarchaeota. Genome Biol. Evol. 6:1549–63
    [Google Scholar]
  40. Elling FJ, Könneke M, Mußmann M, Greve A, Hinrichs K-U 2015. Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates. Geochim. Cosmochim. Acta 171:238–55
    [Google Scholar]
  41. Finn RD, Clements J, Eddy SR 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–37
    [Google Scholar]
  42. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB 2005. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. PNAS 102:14683–88
    [Google Scholar]
  43. Frigaard N, Martinez A, Mincer T, DeLong EF 2006. Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439:847–50
    [Google Scholar]
  44. Fuhrman JA 2011. Oceans of Crenarchaeota: a personal history describing this paradigm shift. Microbe 6:531–37
    [Google Scholar]
  45. Fuhrman JA, Davis AA 1997. Widespread archaea and novel bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar. Ecol. Prog. Ser. 150:275–85
    [Google Scholar]
  46. Fuhrman JA, McCallum K, Davis AA 1992. Novel major archaebacterial group from marine plankton. Nature 356:148–49
    [Google Scholar]
  47. Fuhrman JA, Ouverney CC 1998. Marine microbial diversity studied via 16S rRNA sequences: cloning results from coastal waters and counting of native archaea with fluorescent single cell probes. Aquat. Ecol. 32:3–15
    [Google Scholar]
  48. Fulweiler RW, Emery HE, Heiss EM, Berounsky VM 2011. Assessing the role of pH in determining water column nitrification rates in a coastal system. Estuaries Coasts 34:1095–102
    [Google Scholar]
  49. Galand PE, Gutièrrez-Provecho C, Massana R, Gasol JM, Casamayor EO 2010. Inter-annual recurrence of archaeal assemblages in the coastal NW Mediterranean Sea (Blanes Bay Microbial Observatory). Limnol. Oceanogr. 55:2117–25
    [Google Scholar]
  50. Galand PE, Lovejoy C, Vincent WF 2006. Remarkably diverse and contrasting archaeal communities in a large arctic river and the coastal Arctic Ocean. Aquat. Microb. Ecol. 44:115–26
    [Google Scholar]
  51. Giovannoni SJ, Thrash JC, Temperton B 2014. Implications of streamlining theory for microbial ecology. ISME J 8:1553–65
    [Google Scholar]
  52. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y et al. 2006. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. PNAS 103:18296–301
    [Google Scholar]
  53. Haro-Moreno JM, Rodríguez-Valera F, López-Garcia P, Moreira D, Martin-Cuadrado AB 2017. New insights into marine group III Euryarchaeota, from dark to light. ISME J 11:1102–17
    [Google Scholar]
  54. Heal KR, Qin W, Ribalet F, Bertagnolli AD, Coyote-Maestas W et al. 2017. Two distinct pools of B12 analogs reveal community interdependencies in the ocean. PNAS 114:364–69
    [Google Scholar]
  55. Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C et al. 2005. Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl. Environ. Microbiol. 71:2303–9
    [Google Scholar]
  56. Hollibaugh JT 2017. Oxygen and the activity and distribution of marine Thaumarchaeota. Environ. Microbiol. Rep. 9:186–88
    [Google Scholar]
  57. Hollibaugh JT, Gifford S, Sharma S, Bano N, Moran MA 2011. Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage. ISME J 5:866–78
    [Google Scholar]
  58. Huerta-Cepas J, Serra F, Bork P 2016. ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol. Biol. Evol. 33:1635–38
    [Google Scholar]
  59. Hughes MN 2008. Chemistry of nitric oxide and related species. Methods Enzymol 436:3–19
    [Google Scholar]
  60. Hugoni M, Taib N, Debroas D, Domaizon I, Dufournel IJ et al. 2013. Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters. PNAS 110:6004–9
    [Google Scholar]
  61. Hurley SJ, Elling FJ, Könneke M, Buchwald C, Wankel SD et al. 2016. Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX86 temperature proxy. PNAS 113:7762–67
    [Google Scholar]
  62. Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM et al. 2006. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. PNAS 103:6442–47
    [Google Scholar]
  63. Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL, Armbrust EV 2012. Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335:587–90
    [Google Scholar]
  64. Jacquot JE, Kondo Y, Knapp AN, Moffett JW 2013. The speciation of copper across active gradients in nitrogen-cycle processes in the eastern tropical South Pacific. Limnol. Oceanogr. 58:1387–94
    [Google Scholar]
  65. Ji QX, Babbin AR, Jayakumar A, Oleynik S, Ward BB 2015. Nitrous oxide production by nitrification and denitrification in the Eastern Tropical South Pacific oxygen minimum zone. Geophys. Res. Lett. 42:10755–64
    [Google Scholar]
  66. Karner MB, DeLong EF, Karl DM 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–10
    [Google Scholar]
  67. Kellogg CTE, Deming JW 2009. Comparison of free-living, suspended particle, and aggregate-associated bacterial and archaeal communities in the Laptev Sea. Aquat. Microb. Ecol. 57:1–18
    [Google Scholar]
  68. Kerou M, Offre P, Valledor L, Abby SS, Melcher M et al. 2016. Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers. PNAS 113:E7937–46
    [Google Scholar]
  69. Kim JG, Park SJ, Sinninghe Damsté JS, Schouten S, Rijpstra WIC et al. 2016. Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. PNAS 113:7888–93
    [Google Scholar]
  70. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–46
    [Google Scholar]
  71. Könneke M, Schubert DM, Brown PC, Hügler M, Standfest S et al. 2014. Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation. PNAS 111:8239–44
    [Google Scholar]
  72. Konstantinidis KT, Braff J, Karl DM, DeLong EF 2009. Comparative metagenomic analysis of a microbial community residing at a depth of 4,000 meters at Station ALOHA in the North Pacific Subtropical Gyre. Appl. Environ. Microbiol. 75:5345–55
    [Google Scholar]
  73. Kozlowski JA, Stieglmeier M, Schleper C, Klotz MG, Stein LY 2016. Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J 10:1836–45
    [Google Scholar]
  74. Krupovic M, Spang A, Gribaido S, Forterre P, Schleper C 2011. A thaumarchaeal provirus testifies for an ancient association of tailed viruses with archaea. Biochem. Soc. Trans. 39:82–88
    [Google Scholar]
  75. Labonte JM, Swan BK, Poulos B, Luo HW, Koren S et al. 2015. Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. ISME J 9:2386–99
    [Google Scholar]
  76. Labrenz M, Sintes E, Toetzke F, Zumsteg A, Herndl GJ et al. 2010. Relevance of a crenarchaeotal subcluster related to Candidatus Nitrosopumilus maritimus to ammonia oxidation in the suboxic zone of the central Baltic Sea. ISME J 4:1496–508
    [Google Scholar]
  77. Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B et al. 2007. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. PNAS 104:7104–9
    [Google Scholar]
  78. Li M, Baker BJ, Anantharaman K, Jain S, Breier JA, Dick GJ 2015. Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea. Nat. Commun. 6:8933
    [Google Scholar]
  79. Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S et al. 2015. Determinants of community structure in the global plankton interactome. Science 348:1262073
    [Google Scholar]
  80. Lincoln SA, Wai B, Eppley JM, Church MJ, Summons RE, DeLong EF 2014. Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean. PNAS 111:9858–63
    [Google Scholar]
  81. Liu S, Han P, Hink L, Prosser JI, Wagner M, Brüggemann N 2017. Abiotic conversion of extracellular NH2OH contributes to N2O emission during ammonia oxidation. Environ. Sci. Technol. 51:13122–32
    [Google Scholar]
  82. Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA et al. 2013. Predominant archaea in marine sediments degrade detrital proteins. Nature 496:215–18
    [Google Scholar]
  83. López-Garcia P, López-López A, Moreira D, Rodríguez-Valera F 2001.a Diversity of free-living prokaryotes from a deep-sea site at the Antarctic Polar Front. FEMS Microbiol. Ecol. 36:193–202
    [Google Scholar]
  84. López-Garcia P, Moreira D, López-López A, Rodríguez-Valera F 2001.b A novel haloarchaeal-related lineage is widely distributed in deep oceanic regions. Environ. Microbiol. 3:72–78
    [Google Scholar]
  85. López-García P, Zivanovic Y, Deschamps P, Moreira D 2015. Bacterial gene import and mesophilic adaptation in archaea. Nat. Rev. Microbiol. 13:447–56
    [Google Scholar]
  86. Löscher C, Kock A, Koenneke M, LaRoche J, Bange H, Schmitz-Streit R 2012. Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosciences 9:2419–29
    [Google Scholar]
  87. Luo HW, Tolar BB, Swan BK, Zhang CLL, Stepanauskas R et al. 2014. Single-cell genomics shedding light on marine Thaumarchaeota diversification. ISME J 8:732–36
    [Google Scholar]
  88. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–81
    [Google Scholar]
  89. Martens-Habbena W, Qin W, Horak RE, Urakawa H, Schauer AJ et al. 2015. The production of nitric oxide by marine ammonia-oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger. Environ. Microbiol. 17:2261–74
    [Google Scholar]
  90. Martin-Cuadrado AB, Garcia-Heredia I, Molto AG, Lopez-Ubeda R, Kimes N et al. 2015. A new class of marine Euryarchaeota group II from the Mediterranean deep chlorophyll maximum. ISME J 9:1619–34
    [Google Scholar]
  91. Martin-Cuadrado AB, Rodríguez-Valera F, Moreira D, Alba J, Ivars-Martínez E et al. 2008. Hindsight in the relative abundance, metabolic potential and genome dynamics of uncultivated marine archaea from comparative metagenomic analyses of bathypelagic plankton of different oceanic regions. ISME J 2:865–86
    [Google Scholar]
  92. Martinez-Rey J, Bopp L, Gehlen M, Tagliabue A, Gruber N 2015. Projections of oceanic N2O emissions in the 21st century using the IPSL Earth system model. Biogeosciences 12:4133–48
    [Google Scholar]
  93. Massana R, DeLong EF, Pedros-Alio C 2000. A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl. Environ. Microbiol. 66:1777–87
    [Google Scholar]
  94. Massana R, Murray AE, Preston CM, DeLong EF 1997. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl. Environ. Microbiol. 63:50–56
    [Google Scholar]
  95. Massana R, Unrein F, Rodríguez-Martínez R, Forn I, Lefort T et al. 2009. Grazing rates and functional diversity of uncultured heterotrophic flagellates. ISME J 3:588–96
    [Google Scholar]
  96. Medina LE, Taylor CD, Pachiadaki MG, Henríquez-Castillo C, Ulloa O, Edgcomb VP 2017. A review of protist grazing below the photic zone emphasizing studies of oxygen-depleted water columns and recent applications of in situ approaches. Front. Mar. Sci. 4:105
    [Google Scholar]
  97. Mende DR, Bryant JA, Aylward FO, Eppley JM, Nielsen T et al. 2017. Environmental drivers of a microbial genomic transition zone in the ocean's interior. Nat. Microbiol. 2:1367–73
    [Google Scholar]
  98. Metcalf WW, Griffin BM, Cicchillo RM, Gao J, Janga SC et al. 2012. Synthesis of methylphosphonic acid by marine microbes: a source for methane in the aerobic ocean. Science 337:1104–7
    [Google Scholar]
  99. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF 2007. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9:1162–75
    [Google Scholar]
  100. Moreira D, Rodríguez-Valera F, López-García P 2004. Analysis of a genome fragment of a deep-sea uncultivated Group II euryarchaeote containing 16S rDNA, a spectinomycin-like operon and several energy metabolism genes. Environ. Microbiol. 6:959–69
    [Google Scholar]
  101. Mosier AC, Francis CA 2011. Determining the distribution of marine and coastal ammonia-oxidizing archaea and bacteria using a quantitative approach. Methods Enzymol 486:205–21
    [Google Scholar]
  102. Mosier AC, Lund MB, Francis CA 2012. Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb. Ecol. 64:955–63
    [Google Scholar]
  103. Muñoz-Marín MDC, Luque I, Zubkov MV, Hill PG, Diez J, García-Fernández JM 2013. Prochlorococcus can use the Pro1404 transporter to take up glucose at nanomolar concentrations in the Atlantic Ocean. PNAS 110:8597–602
    [Google Scholar]
  104. Murray AE, Blakis A, Massana R, Strawzewski S, Passow U et al. 1999. A time series assessment of planktonic archaeal variability in the Santa Barbara Channel. Aquat. Microb. Ecol. 20:129–45
    [Google Scholar]
  105. Mußmann M, Brito I, Pitcher A, Sinninghe Damsté JS, Hatzenpichler R et al. 2011. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. PNAS 108:16771–76
    [Google Scholar]
  106. Needham DM, Fuhrman JA 2016. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat. Microbiol. 1:16005
    [Google Scholar]
  107. Nevison C, Butler JH, Elkins J 2003. Global distribution of N2O and the ΔN2O-AOU yield in the subsurface ocean. Glob. Biogeochem. Cycles 17:1119
    [Google Scholar]
  108. Newell SE, Babbin AR, Jayakumar A, Ward BB 2011. Ammonia oxidation rates and nitrification in the Arabian Sea. Glob. Biogeochem. Cycles 25:GB4016
    [Google Scholar]
  109. Newell SE, Fawcett SE, Ward BB 2013. Depth distribution of ammonia oxidation rates and ammonia-oxidizer community composition in the Sargasso Sea. Limnol. Oceanogr. 58:1491–500
    [Google Scholar]
  110. Nishimura Y, Watai H, Honda T, Mihara T, Omae K et al. 2017. Environmental viral genomes shed new light on virus-host interactions in the ocean. mSphere 2:e00359–16
    [Google Scholar]
  111. Nunoura T, Takaki Y, Hirai M, Shimamura S, Makabe A et al. 2015. Hadal biosphere: insight into the microbial ecosystem in the deepest ocean on Earth. PNAS 112:E1230–36
    [Google Scholar]
  112. Orsi WD, Smith JM, Liu S, Liu Z, Sakamoto CM et al. 2016. Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean. ISME J 10:2158–73
    [Google Scholar]
  113. Orsi WD, Smith JM, Wilcox HM, Swalwell JE, Carini P et al. 2015. Ecophysiology of uncultivated marine euryarchaea is linked to particulate organic matter. ISME J 9:1747–63
    [Google Scholar]
  114. Ottesen EA, Young CR, Eppley JM, Ryan JP, Chavez FP et al. 2013. Pattern and synchrony of gene expression among sympatric marine microbial populations. PNAS 110:E488–97
    [Google Scholar]
  115. Ouverney CC, Fuhrman JA 2000. Marine planktonic Archaea take up amino acids. Appl. Environ. Microbiol. 66:4829–33
    [Google Scholar]
  116. Pachiadaki MG, Taylor C, Oikonomou A, Yakimov MM, Stoeck T, Edgcomb V 2016. In situ grazing experiments apply new technology to gain insights into deep-sea microbial food webs. Deep-Sea Res. II 129:223–31
    [Google Scholar]
  117. Palatinszky M, Herbold C, Jehmlich N, Pogoda M, Han P et al. 2015. Cyanate as an energy source for nitrifiers. Nature 524:105–8
    [Google Scholar]
  118. Parada AE, Fuhrman JA 2017. Marine archaeal dynamics and interactions with the microbial community over 5 years from surface to seafloor. ISME J 11:2510–25
    [Google Scholar]
  119. Pearson A, McNichol A, Benitez-Nelson B, Hayes J, Eglinton T 2001. Origins of lipid biomarkers in Santa Monica Basin surface sediment: a case study using compound-specific Δ14C analysis. Geochim. Cosmochim. Acta 65:3123–37
    [Google Scholar]
  120. Peng XF, Fuchsman CA, Jayakumar A, Warner MJ, Devol AH, Ward BB 2016. Revisiting nitrification in the Eastern Tropical South Pacific: a focus on controls. J. Geophys. Res. Oceans 121:1667–84
    [Google Scholar]
  121. Pernthaler A, Preston CM, Pernthaler J, DeLong EF, Amann R 2002. Comparison of fluorescently labeled oligonucleotide and polynucleotide probes for the detection of pelagic marine bacteria and archaea. Appl. Environ. Microbiol. 68:661–67
    [Google Scholar]
  122. Pernthaler J 2005. Predation on prokaryotes in the water column and its ecological implications. Nat. Rev. Microbiol. 3:537–46
    [Google Scholar]
  123. Philosof A, Yutin N, Flores-Uribe J, Sharon I, Koonin EV, Béjà O 2017. Novel abundant oceanic viruses of uncultured marine group II Euryarchaeota. Curr. Biol. 27:1362–68
    [Google Scholar]
  124. Qin W, Amin SA, Lundeen RA, Heal KR, Martens-Habbena W et al. 2017.a Stress response of a marine ammonia-oxidizing archaeon informs physiological status of environmental populations. ISME J 12:508–19
    [Google Scholar]
  125. Qin W, Amin SA, Martens-Habbena W, Walker CB, Urakawa H et al. 2014. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. PNAS 111:12504–9
    [Google Scholar]
  126. Qin W, Meinhardt KA, Moffett JW, Devol AH, Armbrust EV et al. 2017.b Influence of oxygen availability on the activities of ammonia-oxidizing archaea. Environ. Microbiol. Rep. 9:250–56
    [Google Scholar]
  127. Quaiser A, Zivanovic Y, Moreira D, López-García P 2011. Comparative metagenomics of bathypelagic plankton and bottom sediment from the Sea of Marmara. ISME J 5:285–304
    [Google Scholar]
  128. Reysenbach A, Flores G 2008. Electron microscopy encounters with unusual thermophiles helps direct genomic analysis of Aciduliprofundum boonei. Geobiology 6:331–36
    [Google Scholar]
  129. Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB et al. 2016. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537:689–93
    [Google Scholar]
  130. Santoro AE, Buchwald C, McIlvin MR, Casciotti KL 2011. Isotopic composition of N2O produced by marine ammonia-oxidizing archaea. Science 333:1282–85
    [Google Scholar]
  131. Santoro AE, Casciotti KL 2011. Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology, and stable isotope fractionation. ISME J 5:1796–808
    [Google Scholar]
  132. Santoro AE, Casciotti KL, Francis CA 2010. Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ. Microbiol. 12:1989–2006
    [Google Scholar]
  133. Santoro AE, Dupont CL, Richter RA, Craig MT, Carini P et al. 2015. Genomic and proteomic characterization of “Candidatus Nitrosopelagicus brevis”: an ammonia-oxidizing archaeon from the open ocean. PNAS 112:1173–78
    [Google Scholar]
  134. Santoro AE, Saito MA, Goepfert TJ, Lamborg CH, Dupont CL, DiTullio GR 2017. Thaumarchaeal ecotype distributions across the equatorial Pacific Ocean and their potential roles in nitrification and sinking flux attenuation. Limnol. Oceanogr. 62:1984–2003
    [Google Scholar]
  135. Schattenhofer M, Fuchs BM, Amann R, Zubkov MV, Tarran GA, Pernthaler J 2009. Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environ. Microbiol. 11:2078–93
    [Google Scholar]
  136. Schouten S, Hopmans EC, Schefuß E, Sinninghe Damsté JS 2002. Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures. Earth Planet. Sci. Lett. 204:265–74
    [Google Scholar]
  137. Schouten S, Villanueva L, Hopmans EC, van der Meer MT, Sinninghe Damsté JS 2014. Are Marine Group II Euryarchaeota significant contributors to tetraether lipids in the ocean. PNAS 111:E4285
    [Google Scholar]
  138. Shiozaki T, Ijichi M, Isobe K, Hashihama F, Nakamura K-I et al. 2016. Nitrification and its influence on biogeochemical cycles from the equatorial Pacific to the Arctic Ocean. ISME J 10:2184–97
    [Google Scholar]
  139. Sintes E, Bergauer K, De Corte D, Yokokawa T, Herndl GJ 2013. Archaeal amoA gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean. Environ. Microbiol. 15:1647–58
    [Google Scholar]
  140. Sintes E, De Corte D, Haberleitner E, Herndl GJ 2016. Geographic distribution of archaeal ammonia oxidizing ecotypes in the Atlantic Ocean. Front. Microbiol. 7:77
    [Google Scholar]
  141. Sintes E, De Corte D, Ouillon N, Herndl GJ 2015. Macroecological patterns of archaeal ammonia oxidizers in the Atlantic Ocean. Mol. Ecol. 24:4931–42
    [Google Scholar]
  142. Smith JM, Casciotti KL, Chavez FP, Francis CA 2014.a Differential contributions of archaeal ammonia oxidizer ecotypes to nitrification in coastal surface waters. ISME J 8:1704–14
    [Google Scholar]
  143. Smith JM, Chavez FP, Francis CA 2014.b Ammonium uptake by phytoplankton regulates nitrification in the sunlit ocean. PLOS ONE 9:e108173
    [Google Scholar]
  144. Smith JM, Damasheck J, Chavez FP, Francis CA 2016. Factors influencing nitrification rates and the abundance and transcriptional activity of ammonia-oxidizing microorganisms in the dark northeast Pacific Ocean. Limnol. Oceanogr. 61:596–609
    [Google Scholar]
  145. Spang A, Caceres EF, Ettema TJG 2017. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357:eaaf3883
    [Google Scholar]
  146. Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P et al. 2010. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18:331–40
    [Google Scholar]
  147. Stahl DA, de la Torre JR 2012. Physiology and diversity of ammonia-oxidizing archaea. Annu. Rev. Microbiol. 66:83–101
    [Google Scholar]
  148. Steele JA, Countway PD, Xia L, Vigil PD, Beman JM et al. 2011. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J 5:1414–25
    [Google Scholar]
  149. Stewart FJ, Ulloa O, DeLong EF 2012. Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ. Microbiol. 14:23–40
    [Google Scholar]
  150. Stieglmeier M, Mooshammer M, Kitzler B, Wanek W, Zechmeister-Boltenstern S et al. 2014. Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J 8:1135–46
    [Google Scholar]
  151. Swan BK, Chaffin MD, Martinez-Garcia M, Morrison HG, Field EK et al. 2014. Genomic and metabolic diversity of Marine Group I Thaumarchaeota in the mesopelagic of two subtropical gyres. PLOS ONE 9:e95380
    [Google Scholar]
  152. Teira E, Lebaron P, van Aken H, Herndl GJ 2006.a Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic. Limnol. Oceanogr. 51:2131–44
    [Google Scholar]
  153. Teira E, Reinthaler T, Pernthaler A, Pernthaler J, Herndl GJ 2004. Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and archaea in the deep ocean. Appl. Environ. Microbiol. 70:4411–14
    [Google Scholar]
  154. Teira E, van Aken H, Veth C, Herndl GJ 2006.b Archaeal uptake of enantiomeric amino acids in the meso- and bathypelagic waters of the North Atlantic. Limnol. Oceanogr. 51:60–69
    [Google Scholar]
  155. Thrash JC, Seitz KW, Baker BJ, Temperton B, Gillies LE et al. 2017. Metabolic roles of uncultivated bacterioplankton lineages in the northern Gulf of Mexico “dead zone.”. mBio 8:e01017–17
    [Google Scholar]
  156. Tolar BB, Wallsgrove NJ, Popp BN, Hollibaugh JT 2017. Oxidation of urea-derived nitrogen by thaumarchaeota-dominated marine nitrifying communities. Environ. Microbiol. 19:4838–50
    [Google Scholar]
  157. Trimmer M, Chronopoulou PM, Maanoja ST, Upstill-Goddard RC, Kitidis V, Purdy KJ 2016. Nitrous oxide as a function of oxygen and archaeal gene abundance in the North Pacific. Nat. Commun. 7:13451
    [Google Scholar]
  158. Tully BJ, Nelson WC, Heidelberg JF 2012. Metagenomic analysis of a complex marine planktonic thaumarchaeal community from the Gulf of Maine. Environ. Microbiol. 14:254–67
    [Google Scholar]
  159. Turich C, Freeman KH, Bruns MA, Conte M, Jones AD, Wakeham SG 2007. Lipids of marine Archaea: patterns and provenance in the water-column and sediments. Geochim. Cosmochim. Acta 71:3272–91
    [Google Scholar]
  160. Vajrala N, Martens-Habbena W, Sayavedra-Soto LA, Schauer A, Bottomley PJ et al. 2013. Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. PNAS 110:1006–11
    [Google Scholar]
  161. Varela MM, van Aken HM, Sintes E, Herndl GJ 2008. Latitudinal trends of Crenarchaeota and Bacteria in the meso- and bathypelagic water masses of the eastern North Atlantic. Environ. Microbiol. 10:110–24
    [Google Scholar]
  162. Vik DR, Roux S, Brum JR, Bolduc B, Emerson JB et al. 2017. Putative archaeal viruses from the mesopelagic ocean. PeerJ 5:e3428
    [Google Scholar]
  163. Villanueva L, Schouten S, Sinninghe Damsté JS 2015. Depth-related distribution of a key gene of the tetraether lipid biosynthetic pathway in marine Thaumarchaeota. Environ. Microbiol. 17:3527–39
    [Google Scholar]
  164. Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N et al. 2010. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. PNAS 107:8818–23
    [Google Scholar]
  165. Wan XS, Sheng H-X, Dai M, Zhang Y, Shi D et al. 2018. Ambient nitrate switches the ammonium consumption pathway in the euphotic ocean. Nat. Commun. 9:915
    [Google Scholar]
  166. Ward BB 2008. Nitrification in marine systems. Nitrogen in the Marine Environment DG Capone, DA Bronk, MR Mulholland, EJ Carpenter 199–262 Burlington, MA: Academic. , 2nd ed..
    [Google Scholar]
  167. Weber EB, Lehtovirta-Morley LE, Prosser JI, Gubry-Rangin C 2015. Ammonia oxidation is not required for growth of Group 1.1c soil Thaumarchaeota. FEMS Microb. Ecol. 91:fiv001
    [Google Scholar]
  168. Woese CR, Fox GE 1977. Phylogenetic structure of prokaryotic domain: the primary kingdoms. PNAS 74:5088–90
    [Google Scholar]
  169. Woese CR, Kandler O, Wheelis ML 1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. PNAS 87:4576–79
    [Google Scholar]
  170. Wu M, Scott AJ 2012. Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 28:1033–34
    [Google Scholar]
  171. Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J et al. 2006. Archaeal nitrification in the ocean. PNAS 103:12317–22
    [Google Scholar]
  172. Yakimov MM, La Cono V, Smedile F, DeLuca TH, Juarez S et al. 2011. Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (central Mediterranean Sea). ISME J 5:945–61
    [Google Scholar]
  173. Yoshida N, Morimoto H, Hirano M, Koike I, Matsuo S et al. 1989. Nitrification rates and 15N abundances of N2O and NO3 in the western North Pacific. Nature 342:895–97
    [Google Scholar]
  174. Zhang CLL, Xie W, Martin-Cuadrado AB, Rodríguez-Valera F 2015. Marine Group II Archaea, potentially important players in the global ocean carbon cycle. Front. Microbiol. 6:1108
    [Google Scholar]
  175. Zhu C, Wakeham SG, Elling FJ, Basse A, Mollenhauer G et al. 2016. Stratification of archaeal membrane lipids in the ocean and implications for adaptation and chemotaxonomy of planktonic archaea. Environ. Microbiol. 18:4324–36
    [Google Scholar]
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