Physiology and diversity of ammonia-oxidizing archaea

Annual Review of Microbiology

Volumn 66, Issue , 2012, Pages 83-101

  Stahl, David A ^a   De La Torre, José R ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SAN FRANCISCO STATE UNIVERSITY   (United States)

Author keywords

ammonia oxidation; nitrification; nitrogen cycle; Thaumarchaeota

Indexed keywords

AMMONIA; BACTERIAL DNA; BACTERIAL RNA; RNA 16S;

AMMONIA OXIDIZING ARCHAEON; ARTICLE; AUTOTROPH; BACTERIAL GROWTH; GENE SEQUENCE; GENETIC VARIABILITY; HABITAT; HETEROTROPH; MICROBIAL METABOLISM; MIXOTROPHY; NITRIFICATION; NITROSOMONAS EUROPAEA; NONHUMAN; OXIDATION; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; STOICHIOMETRY; THAUMARCHAEOTA;

AMMONIA; ARCHAEA; GENETIC VARIATION; METABOLIC NETWORKS AND PATHWAYS; NITROGEN; OXIDATION-REDUCTION;

NITROSOMONADALES;

EID: 84872250001     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-092611-150128     Document Type: Article

References (85)

1. Allison SM, Prosser JI. 1991. Urease activity in neutrophilic autotrophic ammonia-oxidizing bacteria isolated from acid soils. Soil Biol. Biochem. 23:45-51
2. 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
3. Bernhard AE, Bollmann A. 2010. Estuarine nitrifiers: new players, patterns and processes. Estuar. Coast. Shelf Sci. 88:1-11
4. Bernhard AE, Landry ZC, Blevins A, de la Torre JR, Giblin AE, Stahl DA. 2010. Abundance of ammoniaoxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl. Environ. Microbiol. 76:1285-89
5. Blainey PC, Mosier AC, Potanina A, Francis CA, Quake SR. 2011. Genome of a low-salinity ammoniaoxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6:e16626
6. BoothMS, Stark JM, Rastetter E. 2005. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol. Monogr. 75:139-57
7. 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
8. Burton SAQ, Prosser JI. 2001. Autotrophic ammonia oxidation at low pH through urea hydrolysis. Appl. Environ. Microbiol. 67:2952-57
9. Busiek KK, Margolin W. 2011. Split decision: A thaumarchaeon encoding both FtsZ and Cdv cell division proteins chooses Cdv for cytokinesis. Mol. Microbiol. 82:535-38
10. Button DK, Robertson BR, Lepp PW, Schmidt TM. 1998. A small, dilute-cytoplasm, high-affinity, novel bacterium isolated by extinction culture and having kinetic constants compatible with growth at ambient concentrations of dissolved nutrients in seawater. Appl. Environ. Microbiol. 64:4467-76
11. Canfield DE. 2005. The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33:1-36
12. Church MJ, DeLong EF, Ducklow HW, Karner MB, Preston CM, Karl DM. 2003. Abundance and distribution of planktonic Archaea and Bacteria in the waters west of the Antarctic Peninsula. Limnol. Oceanogr. 48:1893-902
13. Clark LL, Ingall ED, Benner R. 1999. Marine organic phosphorus cycling: novel insights from nuclear magnetic resonance. Am. J. Sci. 299:724-37
14. Crump BC, Baross JA. 2000. Archaeaplankton in the Columbia River, its estuary and the adjacent coastal ocean, USA. FEMS Microbiol. Ecol. 31:231-39
15. Damste JSS, Schouten S, Hopmans EC, van Duin ACT, Geenevasen JAJ. 2002. Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic Crenarchaeota. J. Lipid Res. 43:1641-51
16. de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA. 2008. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 10:810-18
17. DeLong EF. 1992. Archaea in coastal marine environments. Proc. Natl. Acad. Sci. USA 89:5685-89
18. Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, et al. 2010. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol. Ecol. 72:386-94
19. Dodsworth JA, Hungate BA, Hedlund BP. 2011. Ammonia oxidation, denitrification and dissimilatory nitrate reduction to ammonium in two US Great Basin hot springs with abundant ammonia-oxidizing archaea. Environ. Microbiol. 13:2371-86
20. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. 2005. Ubiquity and diversity of ammoniaoxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. USA 102:14683-88
21. Fuhrman JA, McCallum K, Davis AA. 1992. Novel major archaebacterial group from marine plankton. Nature 356:148-49
22. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, et al. 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889-92
23. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y, et al. 2006. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl. Acad. Sci. USA 103:18296-301
24. Hatzenpichler R, Lebecleva EV, Spieck E, Stoecker K, Richter A, et al. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. USA 105:2134-39
25. 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
26. Hershberger KL, Barns SM, Reysenbach AL, Dawson SC, Pace NR. 1996. Wide diversity of Crenarchaeota. Nature 384:420
27. Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM, et al. 2006. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc. Natl. Acad. Sci. USA103:6442-47
28. Jia ZJ, Conrad R. 2009. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11:1658-71
29. Jiang HC, Huang QY, Dong HL, Wang P, Wang FP, et al. 2010. RNA-based investigation of ammoniaoxidizing archaea in hot springs of Yunnan Province, China. Appl. Environ. Microbiol. 76:4538-41
30. Jung MY, Park SJ, Min D, Kim JS, Rijpstra WIC, et al. 2011. Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal Group I. 1a from an agricultural soil. Appl. Environ. Microbiol. 77:8635-47
31. Jurgens G, Lindstrom K, Saano A. 1997. Novel group within the kingdom Crenarchaeota from boreal forest soil. Appl. Environ. Microbiol. 63:803-5
32. Kamat SS, Williams HJ, Raushel FM. 2011. Intermediates in the transformation of phosphonates to phosphate by bacteria. Nature 480:570-73
33. Karl DM, Beversdorf L, Bjorkman KM, Church MJ, Martinez A, DeLong EF. 2008. Aerobic production of methane in the sea. Nat. Geosci. 1:473-78
34. Karner MB, DeLong EF, Karl DM. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507-10
35. Kim BK, Jung MY, Yu DS, Park SJ, Oh TK, et al. 2011. Genome sequence of an ammonia-oxidizing soil archaeon, "Candidatus Nitrosoarchaeum koreensis" MY1. J. Bacteriol. 193:5539-40
36. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543-66
37. Kuypers MMM, Blokker P, Erbacher J, Kinkel H, Pancost RD, et al. 2001. Massive expansion of marine archaea during a mid-Cretaceous oceanic anoxic event. Science 293:92-94
38. Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, et al. 2005. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102:6478-83
39. Kuypers MMM, Sliekers AO, Lavik G, Schmid M, Jorgensen BB, et al. 2003. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422:608-11
40. Lehtovirta LE, Prosser JI, Nicol GW. 2009. Soil pH regulates the abundance and diversity of Group 1. 1c Crenarchaeota. FEMS Microbiol. Ecol. 70:367-76
41. Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW. 2011. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc. Natl. Acad. Sci. USA 108:15892-97
42. Leininger S, Urich T, Schloter M, Schwark L, Qi J, et al. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806-9
43. Lindas A-C, Karlsson EA, Lindgren MT, Ettema TJG, Bernander R. 2008. A unique cell division machinery in the Archaea. Proc. Natl. Acad. Sci. USA 105:18942-46
44. MacGregor BJ, Moser DP, Baker BJ, Alm EW, Maurer M, et al. 2001. Seasonal and spatial variability in Lake Michigan sediment small-subunit rRNA concentrations. Appl. Environ. Microbiol. 67:3908-22
45. Margolin W. 2005. FtsZ and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6:862-72
46. 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
47. Martens-Habbena W, Urakawa H, Costa KC, Gee AM, Stahl DA. 2009. Autotrophy-mixotrophyheterotrophy: clues about the physiology of mesophilic ammonia-oxidizing crenarchaeota. Presented at Am. Soc. Microbiol. Gen. Meet., Philadelphia, PA
48. 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
49. Metcalf WW, van der Donk WA. 2009. Biosynthesis of phosphonic and phosphinic acid natural products. Annu. Rev. Biochem. 78:65-94
50. Mussmann M, Brito I, Pitcher A, Damste JSS, Hatzenpichler R, et al. 2011. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc. Natl. Acad. Sci. USA 108:16771-76
51. Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C. 2003. Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ. Microbiol. 5:787-97
52. OffreP, Prosser JI, NicolGW. 2009. Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol. Ecol. 70:99-108
53. Ouverney CC, Fuhrman JA. 2000. Marine planktonic archaea take up amino acids. Appl. Environ. Microbiol. 66:4829-33
54. Pearson A, Huang Z, Ingalls AE, Romanek CS, Wiegel J, et al. 2004. Nonmarine crenarchaeol in Nevada hot springs. Appl. Environ. Microbiol. 70:5229-37
55. Pearson A, McNichol AP, Benitez-Nelson BC, Hayes JM, Eglinton TI. 2001. Origins of lipid biomarkers in Santa Monica Basin surface sediment: a case study using compound-specific δC14 analysis. Geochim. Cosmochim. Acta 65:3123-37
56. Pelve EA, Lindas AC, Martens-Habbena W, de la Torre JR, Stahl DA, Bernander R. 2011. Cdv-based cell division and cell cycle organization in the thaumarchaeon Nitrosopumilus maritimus. Mol. Microbiol. 82:555-66
57. Pratscher J, Dumont MG, Conrad R. 2011. Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil. Proc. Natl. Acad. Sci. USA 108:4170-75
58. Quinn JP, Kulakova AN, Cooley NA, McGrath JW. 2007. New ways to break an old bond: the bacterial carbon-phosphorus hydrolases and their role in biogeochemical phosphorus cycling. Environ. Microbiol. 9:2392-400
59. Reeburgh WS. 2007. Oceanic methane biogeochemistry. Chem. Rev. 107:486-513
60. Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C. 2008. Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol. Ecol. 64:167-74
61. Samson RY, Bell SD. 2011. Cell cycles and cell division in the archaea. Curr. Opin. Biotechnol. 14:1-7
62. Samson RY, Obita T, Freund SM, Williams RL, Bell SD. 2008. A role for the ESCRT system in cell division in archaea. Science 322:1710-13
63. Santoro AE, Buchwald C, McIlvin MR, Casciotti KL. 2011. Isotopic signature of N2O produced by marine ammonia-oxidizing archaea. Science 333:1282-85
64. Sayavedra-Soto LA, Hamamura N, Liu CW, Kimbrel JA, Chang JH, Arp DJ. 2011. The membraneassociated monooxygenase in the butane-oxidizing gram-positive bacterium Nocardioides sp. strain CF8 is a novel member of the AMO/PMO family. Environ. Microbiol. Rep. 3:390-96
65. Schleper C, Holben W, Klenk HP. 1997. Recovery of crenarchaeotal ribosomal DNA sequences from freshwater-lake sediments. Appl. Environ. Microbiol. 63:321-23
66. Schleper C, Nicol GW. 2010. Ammonia-oxidising archaea: physiology, ecology and evolution. Adv. Microb. Physiol. 57:1-41
67. Scranton MI, Brewer PG. 1977. Occurrence of methane in near-surface waters of western subtropical North-Atlantic. Deep-Sea Res. 24:127-38
68. Seidel HM, Freeman S, Seto H, Knowles JR. 1988. Phosphonate biosynthesis: isolation of the enzyme responsible for the formation of a carbon phosphorus bond. Nature 335:457-58
69. Shao ZY, Blodgett JAV, Circello BT, Eliot AC, Woodyer R, et al. 2008. Biosynthesis of 2-hydroxyethylphosphonate, an unexpected intermediate common to multiple phosphonate biosynthetic pathways. J. Biol. Chem. 283:23161-68
70. Shaw LJ, Nicol GW, Smith Z, Fear J, Prosser JI, Baggs EM. 2006. Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ. Microbiol. 8:214-22
71. 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
72. Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, et al. 1999. Missing lithotroph identified as new planctomycete. Nature 400:446-49
73. Tilbrook BD, Karl DM. 1995. Methane sources, distributions and sinks from California coastal waters to the oligotrophic North Pacific gyre. Mar. Chem. 49:51-64
74. Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, et al. 2011. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl. Acad. Sci. USA 108:8420-25
75. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C. 2005. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic Crenarchaeota in nitrogen cycling. Environ. Microbiol. 7:1985-95
76. Urakawa H, Martens-Habbena W, Stahl DA. 2011. Physiology and genomics of ammonia-oxidizing archaea. In Nitrification, ed. BB Ward, MG Klotz, DJ Arp, pp. 117-55. Washington, DC: ASM Press
77. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74
78. Verhamme DT, Prosser JI, Nicol GW. 2011. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5:1067-71
79. VetrianiC, Reysenbach AL, Dore J. 1998. Recovery and phylogenetic analysis of archaeal rRNA sequences from continental shelf sediments. FEMS Microbiol. Ecol. 161:83-88
80. Walker CB, de la Torre JR, Klotz MG, Urakawa H, PinelN, et al. 2010. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. USA 107:8818-23
81. Winogradsky S. 1890. Recherches sur les organismes de la nitrification. Ann. Inst. Pasteur 4:257-75
82. Wuchter C, Schouten S, Boschker HT, Sinninghe Damste JS. 2003. Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol. Lett. 219:203-7
83. Zhang CL, Ye Q, Huang ZY, Li WJ, Chen JQ, et al. 2008. Global occurrence of archaeal amoA genes in terrestrial hot springs. Appl. Environ. Microbiol. 74:6417-26
84. Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI. 2010. Autotrophic ammonia oxidation by soil thaumarchaea. Proc. Natl. Acad. Sci. USA 107:17240-45
85. Zhao WD, Song ZQ, Jiang HC, Li WJ, Mou XZ, et al. 2011. Ammonia-oxidizing Archaea in Kamchatka Hot Springs. Geomicrobiology J. 28:149-59