Ammonia-oxidizing archaea and bacteria are structured by geography in biological soil crusts across North American arid lands

Ecological Processes

Volumn 2, Issue 1, 2013, Pages 1-10

  Marusenko, Yevgeniy ^a   Bates, Scott T ^b   Anderson, Ian ^a   Johnson, Shannon L ^c   Soule, Tanya ^d   Garcia Pichel, Ferran ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d INDIANA UNIVERSITY PURDUE UNIVERSITY FORT WAYNE   (United States)

Author keywords

Ammonia oxidation; amoA; Arid; Biological soil crust; Desert; Nitrification; Nitrogen cycle; Thaumarchaeota

Indexed keywords

AMMONIA; ARID REGIONS; BIOGEOCHEMISTRY; GENES; LANDFORMS; NITRIFICATION; NITROGEN FERTILIZERS; POLYMERASE CHAIN REACTION; SOILS;

AMMONIA OXIDATION; AMOA; ARID; BIOLOGICAL SOIL CRUSTS; DESERT; NITROGEN CYCLES; THAUMARCHAEOTA;

BACTERIA;

AMMONIA; ARID REGION; DESERT; MICROBIAL ACTIVITY; NITRIFICATION; NITROGEN CYCLE; SOIL ECOSYSTEM; SOIL MICROORGANISM;

CHIHUAHUAN DESERT; COLORADO PLATEAU; GREAT BASIN; SONORAN DESERT; UNITED STATES;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOMONADALES;

EID: 84906698528     PISSN: None     EISSN: 21921709     Source Type: Journal    
DOI: 10.1186/2192-1709-2-9     Document Type: Article

References (92)

1. Adair K. L, Schwartz E (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microb Ecol 56(3):420-426
2. Agogué H., Brink M, Dinasquet J, Herndl GJ (2008) Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456(7223):788-791
3. Auguet J., Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured Archaea. ISME J 4(2):182-190
4. Baker G. C, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55(3):541-555
5. Bartossek R., Nicol GW, Lanzen A, Klenk H, Schleper C (2010) Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context. Environ Microbiol 12(4):1075-1088
6. Bates S. T, Garcia-Pichel F (2009) A culture-independent study of free-living fungi in biological soil crusts of the Colorado Plateau: their diversity and relative contribution to microbial biomass. Environ Microbiol 11(1):56-67
7. Bates S. T, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5(5):908-917
8. Bates S. T, Nash TH III, Garcia-Pichel F (2012) Patterns of diversity for fungal assemblages of biological soil crusts from the southwestern United States. Mycologia 104(2):353-361
9. Belnap J. (1995) Surface disturbances: their role in accelerating desertification. Environ Monit Assess 37(1-3):39-57
10. Belnap J., Lange OL (2003) Biological soil crusts: structure, function, and management. Springer Verlag, Berlin, Germany
11. Blainey P. C, Mosier AC, Potanina A, Francis CA, Quake SR (2011) Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6(2):e16626
12. Campbell J. H, Clark JS, Zak JC (2009) PCR-DGGE Comparison of bacterial community structure in fresh and archived soils sampled along a Chihuahuan Desert elevational gradient. Microb Ecol 57(2):261-266
13. Cao H., Li M, Hong Y, Gu J (2011) Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment. Syst Appl Microbiol 34(7):513-523
14. Chain P., Lamerdin J, Larimer F, Regala W, Lao V, Land M, Hauser L, Hooper A, Klotz M., Norton J, Sayavedra-Soto L, Arciero D, Hommes N, Whittaker M, Arp D. (2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185(9):2759-2773
15. Chen X., Zhu Y, Xia Y, Shen J, He J (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10(8):1978-1987
16. de la Torre JR, Walker CB, Ingalls AE, Koenneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10(3):810-818
17. Di H. J, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621-624
18. Elbert W., Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U. (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5(7):459-462
19. Evans R. D, Johansen JR (1999) Microbiotic crusts and ecosystem processes. Crit Rev Plant Sci 18(2):183-225
20. Fan F., Zhang F, Lu Y (2011) Linking plant identity and interspecific competition to soil nitrogen cycling through ammonia oxidizer communities. Soil Biol Biochem 43(1):46-54
21. Fernandez-Guerra A, Casamayor EO (2012) Habitat-associated phylogenetic community patterns of microbial ammonia oxidizers. PLoS One 7(10):e47330
22. Francis C. A, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102(41):14683-14688
23. French E., Kozlowski JA, Mukherjee M, Bullerjahn G, Bollmann A (2012) Ecophysiological characterization of ammonia-oxidizing archaea and bacteria from freshwater. Appl Environ Microbiol 78(16):5773-5780
24. Fu B. J, Zhang QJ, Chen LD, Zhao WW, Gulinck H, Liu GB, Yang QK, Zhu YG (2006) Temporal change in land use and its relationship to slope degree and soil type in a small catchment on the Loess Plateau of China. Catena 65(1):41-48
25. Garcia-Pichel F, Belnap J (1996) Microenvironments and microscale productivity of cyanobacterial desert crusts. J Phycol 32(5):774-782
26. Garcia-Pichel F, Lopez-Cortes A, Nubel U (2001) Phylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado Plateau. Appl Environ Microbiol 67(4):1902-1910
27. Garcia-Pichel F, Johnson SL, Youngkin D, Belnap J (2003) Small-scale vertical distribution of bacterial biomass and diversity in biological soil crusts from arid lands in the Colorado Plateau. Microb Ecol 46(3):312-321
28. Garcia-Pichel F, Wojciechowski MF (2009) The evolution of a capacity to build supra-cellular ropes enabled filamentous cyanobacteria to colonize highly erodible substrates. PLoS One 4(11):e7801
29. Glaser K., Hackl E, Inselsbacher E, Strauss J, Wanek W, Zechmeister-Boltenstern S, Sessitsch A. (2010) Dynamics of ammonia-oxidizing communities in barleyplanted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol Ecol 74(3):575-591
30. Gleeson D. B, Mueller C, Banerjee S, Ma W, Siciliano SD, Murphy DV (2010) Response of ammonia oxidizing archaea and bacteria to changing water filled pore space. Soil Biol Biochem 42(10):1888-1891
31. Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74(3):566-574
32. Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths R. I, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci USA 108(52):21206-21211
33. Gundlapally S. R, Garcia-Pichel F (2006) The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol 52(2):345-357
34. Hallam S. J, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM, DeLong EF (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 4(4):E95
35. Hallin S., Jones CM, Schloter M, Philippot L (2009) Relationship between N cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597-605
36. Hammer Ø., Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electr 4:1-9
37. Hatzenpichler R. (2012) Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol 78(21):7501-7510
38. Hatzenpichler R., Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci USA 105(6):2134-2139
39. He J., Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, Di H (2007) 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 9(9):2364-2374
40. Hocking R. (1976) Analysis and selection of variables in linear-regression. Biometrics 32(1):1-49
41. Johnson S. L, Budinoff CR, Belnap J, Garcia-Pichel F (2005) Relevance of ammonium oxidation within biological soil crust communities. Environ Microbiol 7(1):1-12
42. Johnson S. L, Neuer S, Garcia-Pichel F (2007) Export of nitrogenous compounds due to incomplete cycling within biological soil crusts of arid lands. Environ Microbiol 9(3):680-689
43. Jung J., Yeom J, Kim J, Han J, Lim HS, Park H, Hyun S, Park W (2011) Change in gene abundance in the nitrogen biogeochemical cycle with temperature and nitrogen addition in Antarctic soils. Res Microbiol 162(10):1018-1026
44. Katoh K., Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14):3059-3066
45. Kim J., Jung M, Park S, Rijpstra WIC, Damste JSS, Madsen EL, Min D, Kim J, Kim G, Rhee S. (2012) Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environ Microbiol 14(6):1528-1543
46. Klappenbach J. A, Saxman PR, Cole JR, Schmidt TM (2001) rrndb: the Ribosomal RNA Operon Copy Number Database. Nucleic Acids Res 29(1):181-184
47. Konneke M., Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl D. A (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437(7058):543-546
48. Lehtovirta L. E, Prosser JI, Nicol GW (2009) Soil pH regulates the abundance and diversity of Group 1.1c Crenarchaeota. FEMS Microbiol Ecol 70(3):367-376
49. 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(38):1-6
50. Leininger S., Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442(7104):806-809
51. Liu Y., Zheng Y, Shen J, Zhang L, He J (2010) Effects of mercury on the activity and community composition of soil ammonia oxidizers. Environ Sci Pollut Res 17(6):1237-1244
52. Mao Y., Yannarell AC, Mackie RI (2011) Changes in N-transforming archaea and bacteria in soil during the establishment of bioenergy crops. PLoS One 6(9):e24750. doi:10.1371/journal.pone.0024750
53. 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(7266):976-979
54. Marusenko Y., Huber DP, Hall SJ (2013) Fungi mediate nitrous oxide production but not ammonia oxidation in aridland soils of the southwestern US. Soil Biol Biochem 63:24-36.
55. Matsutani N., Nakagawa T, Nakamura K, Takahashi R, Yoshihara K, Tokuyama T (2011) Enrichment of a novel marine ammonia-oxidizing archaeon obtained from sand of an eelgrass zone. Microb Environ 26(1):23-29
56. Mosier A. C, Francis CA (2008) Relative abundance and diversity of ammoniaoxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10:3002-3016
57. Mosier A. C, Lund MB, Francis CA (2012) Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb Ecol 64(4):955-963
58. Nagy M. L, Perez A, Garcia-Pichel F (2005) The prokaryotic diversity of biological soil crusts in the Sonoran Desert (Organ Pipe Cactus National Monument, AZ). FEMS Microbiol Ecol 54(2):233-245
59. Nannipieri P., Eldor P (2009) The chemical and functional characterization of soil N and its biotic components. Soil Biol Biochem 41(12):2357-2369
60. Nicol G. W, Prosser JI (2011) Strategies to determine diversity, growth and activity of ammonia oxidising archaea in soil. Methods Enzymol 496:3-34
61. Norton J. M, Alzerreca JJ, Suwa Y, Klotz MG (2002) Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Arch Microbiol 177(2):139-149
62. 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(9):787-797
63. Palmer M. W (1993) Putting things in even better order-the advantages of canonical correspondence-analysis. Ecology 74(8):2215-2230
64. Park B., Park S, Yoon D, Schouten S, Damste JSS, Rhee S (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol 76(22):7575-7587
65. Pester M., Rattei T, Flechl S, Groengroeft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammoniaoxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14(2):525-539
66. Pointing S. B, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10(8):551-562
67. Prosser J. I, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20 (11):523-531
68. Rotthauwe J. H, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63(12):4704-4712
69. Safriel U., Adeel Z, Niemeijer D, Puigdefabregas J, White R, Lal R, Winslow M, Ziedler J., Prince S, Archer E, King C (2005) Dryland systems. In: Hassan R, Scholes R. J, Ash N (eds) Ecosystems and human well-being. Findings of the Conditions and Trends Working Group of the Millennium Ecosystem Assessment. Island Press, Washington DC, pp 623-662
70. Santoro A. E, Casciotti KL (2011) Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. ISME J 5(11):1796-1808
71. Schimel J. P, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85(3):591-602
72. Schleper C., Nicol GW (2010) Ammonia-oxidising archaea-physiology, ecology and evolution. Adv Microb Physiol 57(57):1-41
73. Schlesinger W. H (1997) Biogeochemistry: an analysis of global change. Academic, San Diego, USA
74. Shen J., Zhang L, Zhu Y, Zhang J, He J (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10(6):1601-1611
75. Smith A. C, Koper N, Francis CM, Fahrig L (2009) Confronting collinearity: comparing methods for disentangling the effects of habitat loss and fragmentation. Landscape Ecol 24(10):1271-1285
76. Soule T., Anderson IJ, Johnson SL, Bates ST, Garcia-Pichel F (2009) Archaeal populations in biological soil crusts from arid lands in North America. Soil Biol Biochem 41(10):2069-2074
77. Stahl D. A, de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83-101
78. Strauss S. L, Day TA, Garcia-Pichel F (2012) Nitrogen cycling in desert biological soil crusts across biogeographic regions in the Southwestern United States. Biogeochemistry 108(1-3):171-182
79. Tamura K., Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731-2739
80. Ter Braak CJF (1986) Canonical correspondence-analysis-a new eigenvector technique for multivariate direct gradient analysis. Ecology 67(5):1167-1179
81. Tourna M., Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10(5):1357-1364
82. Tourna M., Stieglmeier M, Spang A, Koenneke M, Schintlmeister A, Urich T, Engel M., Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108(20):8420-8425
83. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11(3):296-310
84. Venter J. C, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I., Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K., White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C., Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304(5667):66-74
85. Walker C. B, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PSG, Chan PP, Gollabgir A, Hemp J, Huegler M, Karr EA, Koenneke M, Shin M, Lawton TJ, Lowe T, Martens-Habbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107(19):8818-8823
86. Wall D. H, Virginia RA (1999) Controls on soil biodiversity: insights from extreme environments. Appl Soil Ecol 13(2):137-150
87. Xu M., Schnorr J, Keibler B, Simon HM (2012) Comparative analysis of 16S rRNA and amoA genes from archaea selected with organic and inorganic amendments in enrichment culture. Appl Environ Microbiol 78(7):2137-2146
88. Ye L., Zhang T (2011) Ammonia-oxidizing bacteria dominates over ammoniaoxidizing archaea in a saline nitrification reactor under low DO and high nitrogen loading. Biotechnol Bioeng 108(11):2544-2552
89. Zeglin L. H, Taylor AE, Myrold DD, Bottomley PJ (2011) Bacterial and archaeal amoA gene distribution covaries with soil nitrification properties across a range of land uses. Environ Microbiol Rep 3(6):717-726
90. Zhang L., Wang M, Prosser JI, Zheng Y, He J (2009) Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol Ecol 70(2):52-61
91. Zhang L. M, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci U. SA 107(40):17240-17245
92. Zhang X., Liu W, Bai Y, Zhang G, Han X (2011) Nitrogen deposition mediates the effects and importance of chance in changing biodiversity. Mol Ecol 20(2):429-438