Archaeal and bacterial ammonia-oxidisers in soil: The quest for niche specialisation and differentiation

Trends in Microbiology

Volumn 20, Issue 11, 2012, Pages 523-531

  Prosser, James I ^a   Nicol, Graeme W ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Ammonia oxidising archaea; Ammonia oxidising bacteria; Mixotrophy; Niche differentiation; Niche specialisation; Nitrification; Soil pH

Indexed keywords

AMMONIA;

AMMONIA OXIDIZING ARCHAEON; AMMONIA OXIDIZING BACTERIUM; ARCHAEAL GENOME; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM CULTURE; COMPETITIVE ABILITY; CONCENTRATION (PARAMETERS); ECOLOGICAL NICHE; ECOLOGICAL SPECIALIZATION; ENVIRONMENTAL FACTOR; FIELD STUDY; GENE EXPRESSION REGULATION; GENE SEQUENCE; MESOCOSM; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROCOSM; MIXOTROPH; MOLECULAR PHYLOGENY; NITRIFICATION; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; REVIEW; SOIL ACIDITY; SPATIAL SOIL VARIABILITY; SPECIES COMPARISON; SPECIES CULTIVATION;

AMMONIA; ARCHAEA; BACTERIA; BIOTA; NITRIFICATION; OXIDATION-REDUCTION; SOIL MICROBIOLOGY;

ARCHAEA; BACTERIA (MICROORGANISMS);

EID: 84867901720     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2012.08.001     Document Type: Review

References (70)

1. Venter J.C., et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004, 304:66-74.
2. Treusch A.H., et al. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ. Microbiol. 2005, 7:1985-1995.
3. Könneke M., et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437:543-546.
4. Brochier-Armanet C., et al. Mesophilic crenarchaeota. Proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 2008, 6:245-252.
5. Leininger S., et al. Archaea predominate among ammonia-oxidising prokaryotes in soils. Nature 2006, 442:806-809.
6. He J.-Z., et al. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 2007, 9:2364-2374.
7. Nicol G.W., et al. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 2008, 10:2966-2978.
8. Prosser J.I., Nicol G.W. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 2008, 10:2931-2941.
9. Erguder T.H., et al. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol. Rev. 2009, 33:855-869.
10. Valentine D.L. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat. Rev. Microbiol. 2007, 5:316-323.
11. Tourna M., et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:8420-8425.
12. Jung M.-Y., et al. Enrichment of an autotrophic ammonia-oxidizing archaeon of thaumarchaeal group I.1a from an agricultural soil. Appl. Environ. Microbiol. 2011, 77:8635-8647.
13. Lehtovirta-Morley L.E., et al. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:15892-15897.
14. Kim J.G., et al. Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environ. Microbiol. 2012, 14:1528-1543.
15. Norton J.M., et al. Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Appl. Environ. Microbiol. 2008, 74:3559-3572.
16. Chain P., et al. Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J. Bacteriol. 2003, 185:2759-2773.
17. Kim J.G., et al. Genome sequence of an ammonia-oxidizing soil archaeon, 'Candidatus Nitrosoarchaeum koreensis' MY1. J. Bacteriol. 2012, 193:5539-5540.
18. Martens-Habbena W., et al. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 2009, 461:976-979.
19. Belser L.W., et al. Growth and oxidation-kinetics of 3 genera of ammonia oxidizing nitrifiers. FEMS Microbiol. Lett. 1980, 7:213-216.
20. Jiang Q.Q., Bakken L.R. Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiol. Ecol. 1999, 30:171-186.
21. Anthonisen A.C., et al. Inhibition of nitrification by ammonia and nitrous acid. J. Water Poll. Control Fed. 1976, 48:835-852.
22. Park S., Bae W. Modeling kinetics of ammonium oxidation and nitrite oxidation under simultaneous inhibition by free ammonia and free nitrous acid. Process Biochem. 2009, 6:631-640.
23. Wertz S., et al. Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiol. Ecol. 2012, 79:142-154.
24. Petersen D.G., et al. Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ. Microbiol. 2012, 14:993-1008.
25. Huaiying Y., et al. Links between ammonia oxidizer community structure, abundance and nitrification potential in acidic soils. Appl. Environ. Microbiol. 2011, 77:4618-4625.
26. 2O emissions. J. Soils Sed. 2011, 11:1399-1407.
27. Zeglin L.H., et al. Bacterial and archaeal amoA gene distribution covaries with soil nitrification properties across a range of land uses. Environ. Microbiol. Rep. 2011, 6:717-726.
28. Stark J.M., Firestone M.K. Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland-annual grassland. Soil Biol. Biochem. 1996, 28:1307-1317.
29. Jia Z., Conrad R. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 2009, 11:1658-1671.
30. 2 fixation by archaea and bacteria in an agricultural soil. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:4170-4175.
31. Di H.J., et al. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2009, 2:621-624.
32. Di H.J., et al. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol. Ecol. 2010, 72:386-394.
33. Koops H.-P., Pommerening-Röser A. Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol. Ecol. 2001, 72:1-9.
34. Webster G., et al. Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ. Microbiol. 2005, 7:676-684.
35. Verhamme D.T., et al. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 2011, 6:1067-1071.
36. Stopnišek N., et al. Thaumarchaeal ammonia oxidation in an acidic forest peat soil is not influenced by ammonium amendment. Appl. Environ. Microbiol. 2010, 76:7626-7634.
37. Levičnik-Höfferle S., et al. Stimulation of thaumarchaeal ammonia oxidation by mineralised organic nitrogen, but not inorganic nitrogen. FEMS Microbiol. Ecol. 2012, 80:114-123.
38. Berg I.A., et al. Autotrophic carbon fixation in archaea. Nat. Rev. Microbiol. 2010, 8:447-460.
39. Norton J.M., et al. Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Arch. Microbiol. 2002, 177:139-149.
40. Walker C.B., et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. U.S.A. 2011, 107:8818-8823.
41. Blainey P.C., et al. Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS ONE 2011, 6:e16626.
42. 2 assimilation genes in autotrophic bacteria. FEMS Microbiol. Rev. 1997, 21:135-155.
43. Sayavedra-Soto L.A., Arp D.J. Ammonia-oxidizing bacteria: their biochemistry and molecular biology. Nitrification 2011, 11-37. ASM Press. B.B. Ward (Ed.).
44. Schmidt I. Chemoorganoheterotrophic growth of Nitrosomonas europaea and Nitrosomonas eutropha. Curr. Microbiol. 2009, 59:130-138.
45. Karlsson A.E. Archaeal abundance in relation to root and fungal exudation rates. FEMS Microbiol. Ecol. 2012, 80:305-311.
46. Kelly J.J., et al. Distinct responses in ammonia-oxidizing archaea and bacteria after addition of biosolids to an agricultural soil. Appl. Environ. Microbiol. 2011, 77:6551-6558.
47. Zhang L.-M., et al. Autotrophic ammonia oxidation by soil thaumarchaea. Proc. Natl Acad. Sci. U.S.A. 2010, 107:17240-17245.
48. Zhang L.-M., et al. Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J. 2012, 6:1032-1045.
49. Xia W., et al. Autotrophic growth of nitrifying community in an agricultural soil. ISME J. 2011, 5:1226-1236.
50. Booth M.S., et al. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol. Monogr. 2005, 75:139-157.
51. Allison S.M., Prosser J.I. Survival of ammonia oxidising bacteria in air-dried soil. FEMS Microbiol. Lett. 1991, 79:65-68.
52. de Boer W., et al. Nitrification at low pH by aggregated autotrophic bacteria. Appl. Environ. Microbiol. 1991, 57:3600-3604.
53. Burton S.A.Q., Prosser J.I. Autotrophic ammonia oxidation at low pH through urea hydrolysis. Appl. Environ. Microbiol. 2001, 67:2952-2957.
54. de Boer W., Laanbroek H.J. Ureolytic nitrification at low pH by Nitrosospira spec. Arch. Microbiol. 1989, 152:178-181.
55. Isobe K., et al. High abundance of ammonia-oxidizing archaea in acidified subtropical forest soils in southern China after long-term N deposition. FEMS Microbiol. Ecol. 2012, 80:193-203.
56. Wessen E., et al. Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl. Soil Ecol. 2011, 45:193-200.
57. Boyle-Yarwood S.A., et al. Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ. Microbiol. 2008, 10:2956-2965.
58. Szukics U., et al. Rapid and dissimilar response of ammonia oxidizing archaea and bacteria to nitrogen and water amendment in two temperate forest soils. Microbiol. Res. 2011, 167:103-109.
59. Cao P., et al. Distribution and diversity of archaeal communities in selected Chinese soils. FEMS Microbiol. Ecol. 2012, 80:146-158.
60. Zhang L.-M., et al. Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol. Ecol. 2009, 70:208-217.
61. Bru D., et al. Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J. 2011, 5:532-542.
62. Pester M., et al. amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ. Microbiol. 2012, 14:525-539.
63. Gubry-Rangin C., et al. Niche specialization of terrestrial archaeal ammonia oxidizers. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:21206-21211.
64. Gubry-Rangin C., et al. Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol. Ecol. 2010, 74:566-574.
65. Offre P., et al. Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol. Ecol. 2009, 70:99-108.
66. Taylor A.E., et al. Evidence for different contributions of archaea and bacteria to the ammonia-oxidizing potential of diverse Oregon soils. Appl. Environ. Microbiol. 2010, 76:7691-7698.
67. Loescher C.R., et al. Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosci. Discuss. 2012, 9:2095-2122.
68. 2O produced by marine ammonia-oxidizing archaea. Science 2011, 333:1282-1285.
69. Prosser J.I. Autotrophic nitrification in bacteria. Adv. Microb. Physiol. 1989, 30:125-181.
70. Koper T.E., et al. Nitrification exhibits Haldane kinetics in an agricultural soil treated with ammonium sulfate or dairy-waste compost. FEMS Microbiol. Ecol. 2010, 74:316-322.