Spatial and temporal diversity and abundance of ammonia oxidizers in semi-arid and arid soils: Indications for a differential seasonal effect on archaeal and bacterial ammonia oxidizers

FEMS Microbiology Ecology

Volumn 86, Issue 3, 2013, Pages 544-556

  Sher, Yonatan ^a   Zaady, Eli ^b   Nejidat, Ali ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b VOLCANI CENTER   (Israel)

Author keywords

Ammonia oxidizing archaea; Ammonia oxidizing bacteria; Desert ecosystems; Inorganic nitrogen

Indexed keywords

ABUNDANCE; AMMONIA; ARID REGION; ARIDITY; BACTERIUM; BIOMASS; COMMUNITY STRUCTURE; DESERT; ELECTROKINESIS; GENE; INORGANIC NITROGEN; LIMITING FACTOR; OXIDATION; SEMIARID REGION; SOIL TYPE; WINTER;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOMONADALES;

AMMONIA; NITROGEN; RNA 16S;

AMMONIA-OXIDIZING ARCHAEA; AMMONIA-OXIDIZING BACTERIA; ARCHAEON; ARTICLE; BACTERIUM; CLASSIFICATION; DENATURING GRADIENT GEL ELECTROPHORESIS; DESERT CLIMATE; DESERT ECOSYSTEMS; GENETICS; INORGANIC NITROGEN; ISRAEL; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHYLOGENY; SEASON;

AMMONIA-OXIDIZING ARCHAEA; AMMONIA-OXIDIZING BACTERIA; DESERT ECOSYSTEMS; INORGANIC NITROGEN;

AMMONIA; ARCHAEA; BACTERIA; DENATURING GRADIENT GEL ELECTROPHORESIS; DESERT CLIMATE; ISRAEL; NITROGEN; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEASONS; SOIL MICROBIOLOGY;

EID: 84887617457     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12180     Document Type: Article

References (79)

1. Adair KL & Schwartz E (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semi-arid soils of northern Arizona, USA. Microb Ecol 56: 420-426.
2. Andrew DR, Fitak RR, Munguia-Vega A, Racolta A, Martinson VG & Dontsovag K (2012) Abiotic factors shape microbial diversity in Sonoran Desert soils. Appl Environ Microbiol 78: 7527-7537.
3. Angel R, Asaf L, Ronen Z & Nejidat A (2010) Nitrogen transformations and diversity of ammonia-oxidizing bacteria in a desert ephemeral stream receiving untreated wastewater. Microb Ecol 59: 46-58.
4. Avrahami S & Conrad R (2003) Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Appl Environ Microbiol 69: 6152-6164.
5. 2O release and on the community structure of ammonia oxidizers and denitrifiers. Appl Environ Microbiol 68: 5685-5692.
6. Avrahami S, Liesack W & Conrad R (2003) Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ Microbiol 5: 691-705.
7. Belnap J, Welter JR, Grimm NB, Barger N & Ludwig JA (2005) Linkages between microbial and hydrologic processes in arid and semi-arid watersheds. Ecology 86: 298-307.
8. Ben-David EA, Zaady E, Sher Y & Nejidat A (2011) Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses. FEMS Microbiol Ecol 76: 492-503.
9. Bernhard AE, Landry ZC, Blevins A, de la Torre JR, Giblin AE & Stahl DA (2010) Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol 76: 1285-1289.
10. Boeken B & Zaady E (2012) Daily Meteorological Measurements Park Shaked 1999 to 2012. Rangeland Ecology Laboratory, BIDR, Ben Gurion University of the Negev Press, Beer Shava, Israel.
11. Boyle-Yarwood SA, Bottomley PJ & Myrold DD (2008) Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ Microbiol 10: 2956-2965.
12. Bruins H (1990) The impact of man and climate on the central Negev and northeastern Sinai deserts during the late Holocene. In Mans Role in the Shaping of the Eastern Mediterranean Landscape (Bottema S, Enjes-Nieborg G & van zeist W, eds), pp. 87-99. Balkema, Rotterdam, the Netherlands.
13. Christensen JH, Hewitson B, Busuioc A et al. (2007) Regional climate projections. Climate Change 2007: The Physical Science Basis (Contribution of Working group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change). Cambridge University Press, Cambridge, UK and New York, NY.
14. Clesceri LS, Greenberg AE & Eaton AD (1998) Standard Methods for the Examination of Water and Wastewater (APHA). Port City Press, Baltimore, MD.
15. 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: 810-818.
16. 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: 2371-2386.
17. Easterling D, Meehl G, Parmesan C, Changnon S, Karl T & Mearns L (2000) Climate extremes: observations, modeling, and impacts. Science 289: 2068-2074.
18. Erguder TH, Boon N, Wittebolle L, Marzorati M & Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33: 855-869.
19. Evans R & Ehleringer J (1994) Water and nitrogen dynamics in an arid woodland. Oecologia 99: 233-242.
20. Evans R & Lange O (2003) Biological soil crusts and ecosystem nitrogen and carbon dynamics. Biological Soil Crusts: Structure, Function, and Management (Benlap J & Lange OL, eds), pp. 263-279. Springer-Verlag, Berlin, Heidelberg.
21. Ferree MA & Shannon RD (2001) Evaluation of a second derivative UV/visible spectroscopy technique for nitrate and total nitrogen analysis of wastewater samples. Water Res 35: 327-332.
22. Flieβach A, Sarig S & Steinberger Y (1994) Effects of water pulses and climatic conditions on microbial biomass kinetics and microbial activity in a Yermosol of the central Negev. Arid Soil Res Rehabil 8: 353-362.
23. Francis C, Roberts K, Beman J, Santoro A & Oakley B (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. P Natl Acad Sci USA 102: 14683-14688.
24. Garcia-Pichel F & Belnap J (1996) Microenvironments and microscale productivity of cyanobacterial desert crusts. J Phycol 32: 774-782.
25. Hart S (2006) Potential impacts of climate change on nitrogen transformations and greenhouse gas fluxes in forests: a soil transfer study. Global Change Biol 12: 1032-1046.
26. Hatzenpichler R (2012) Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol 78: 7501-7510.
27. 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. P Natl Acad Sci USA 105: 2134-2139.
28. 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: 2364-2374.
29. Herman R, Provencio K, Herreramatos J & Torrez R (1995) Resource islands predict the distribution of heterotrophic bacteria in Chihuahuan desert soils. Appl Environ Microbiol 61: 1816-1821.
30. Hooper D, Chapin F, Ewel J et al. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75: 3-35.
31. Horz H, Barbrook A, Field C & Bohannan B (2004) Ammonia-oxidizing bacteria respond to multifactorial global change. P Natl Acad Sci USA 101: 15136-15141.
32. Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K & Johnson CA (2001) Climate Change 2001: The Scientific Basis. Cambridge University Press, Cambridge.
33. Issa O, Stal L, Defarge C, Coute A & Trichet J (2001) Nitrogen fixation by microbial crusts from desiccated Sahelian soils (Niger). Soil Biol Biochem 33: 1425-1428.
34. Jia Z & Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11: 1658-1671.
35. Jiang Q & Bakken L (1999) Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiol Ecol 30: 171-186.
36. Kalfe HK & Bruins HJ (2009) Climatic trends in Israel 1970-2002: warmer and increasing aridity inland. Clim Change 96: 63-77.
37. Kidron GJ (2010) Under-canopy microclimate within sand dunes in the Negev Desert. J Hydrol 392: 201-210.
38. Koops H, Purkhold U, Pommerening-Röser A, Timmermann G, Wagner M (2003) The lithoautotrophic ammonia-oxidizing bacteria. The Prokaryotes: An Evolving Electronic Resource for the Microbiology Community, 3rd edn, Release 3.13 (Dworkin M, Falkow S, Rosenberg E, Schleifer K-H & Stackebrandt E, eds), pp. 778-811. Springer, New York.
39. Le Houerou H (1996) Climate change, drought and desertification. J Arid Environ 34: 133-185.
40. 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: 806-809.
41. Mahmood S, Freitag TE & Prosser JI (2006) Comparison of PCR primer-based strategies for characterization of ammonia oxidizer communities in environmental samples. FEMS Microbiol Ecol 56: 482-493.
42. Malchair S, De Boeck HJ, Lemmens CMHM, Merckx R, Nijs I, Ceulemans R & Carnol M (2010) Do climate warming and plant species richness affect potential nitrification, basal respiration and ammonia-oxidizing bacteria in experimental grasslands? Soil Biol Biochem 42: 1944-1951.
43. Mazor G, Kidron GJ, Vonshak A & Abeliovich A (1996) The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiol Ecol 21: 121-130.
44. Millennium Ecosystem Assessment (2005) Ecosystems and Human Well-being: Desertification Synthesis. World Resources Institute, Washington, DC.
45. Nejidat A (2005) Nitrification and occurrence of salt-tolerant nitrifying bacteria in the Negev desert soils. FEMS Microbiol Ecol 52: 21-29.
46. Nelson DW & Sommers LE (1996) Total carbon, organic carbon, and organic matter. Methods of Soil Analysis Part 3 - Chemical Methods (Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT & Sumner ME, eds), pp. 961-1010. Soil Science Society of America, American Society of Agronomy, Madison, WI.
47. Nicol GW, Leininger S, Schleper C & Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia -oxidizing archaea and bacteria. Environ Microbiol 10: 2966-2978.
48. Orlando J, Alfaro M, Bravo L, Guevara R & Caru M (2010) Bacterial diversity and occurrence of ammonia-oxidizing bacteria in the Atacama Desert soil during a "desert bloom" event. Soil Biol Biochem 42: 1183-1188.
49. Parker SS & Schimel JP (2011) Soil nitrogen availability and transformations differ between the summer and the growing season in a California grassland. Appl Soil Ecol 48: 185-192.
50. Pereira E Silva M, Poly F, Guillaumaud N, van Elsas JD & Salles JF (2012) Fluctuations in ammonia- oxidizing communities across agricultural soils are driven by soil structure and pH. Front Microbiol 3: 77.
51. Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M & Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14: 993-1008.
52. Prosser JI & Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10: 2931-2941.
53. Prosser JI & Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20: 523-531.
54. Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops H-P & Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66: 5368-5382.
55. 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: 167-174.
56. Sarig S & Steinberger Y (1994) Microbial biomass response to seasonal fluctuation in soil salinity under the canopy of desert halophytes. Soil Biol Biochem 26: 1405-1408.
57. Schwinning S, Davis K, Richardson L & Ehleringer J (2002) Deuterium enriched irrigation indicates different forms of rain use in shrub/grass species of the Colorado Plateau. Oecologia 130: 345-355.
58. Seager R, Ting M, Held I et al. (2007) Model projections of an imminent transition to a more arid climate in southwestern North America. Science 316: 1181-1184.
59. Seyfried M, Schwinning S, Walvoord M, Pockman W, Newman B, Jackson R & Phillips FM (2005) Ecohydrological control of deep drainage in arid and semi-arid regions. Ecology 86: 277-287.
60. Shaver G, Canadell J, Chapin F et al. (2000) Global warming and terrestrial ecosystems: a conceptual framework for analysis. Bioscience 50: 871-882.
61. 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: 1601-1611.
62. Sher Y, Zaady E, Ronen Z & Nejidat A (2012) Nitrification activity and levels of inorganic nitrogen in soils of a semi-arid ecosystem following a drought-induced shrub death. Eur J Soil Biol 53: 86-93.
63. Skujins J (1984) Microbial ecology of desert soils. Adv Microb Ecol 7: 49-91.
64. Stark J & Firestone M (1995) Mechanisms for soil-moisture effects on activity of nitrifying bacteria. Appl Environ Microbiol 61: 218-221.
65. Stern A, Gradus Y, Meir A, Krakover S & Tsoar H (1986) Atlas of the Negev. Ben-Gurion of the Negev, Beer-Sheva.
66. Sullivan BW, Selmants PC & Hart SC (2012) New evidence that high potential nitrification rates occur in soils during dry seasons: are microbial communities metabolically active during dry seasons? Soil Biol Biochem 53: 28-31.
67. Tamura K, Dudley J, Nei M & Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
68. Teomim N (1990) Soil Survey of the Sayeret Shaked Park. Jewish National Fund, Gilat, Israel.
69. van de Vossenberg J, Driessen A & Konings W (1998) The essence of being extremophilic: the role of the unique archaeal membrane lipids. Extremophiles 2: 163-170.
70. Walvoord MA, Phillips FM, Stonestrom DA, Evans RD, Hartsough PC, Newman BD & Striegl RG (2003) A reservoir of nitrate beneath desert soils. Science 302: 1021-1024.
71. Wardle DA, Brown VK, Behan-Pelletier V et al. (2004) Vulnerability to global change of ecosystem goods and services driven by soil biota. Sustaining Biodiversity and Ecosystem Services in Soils and Sediments (Wall DH, ed.), pp. 101-136. Island Press, Washington, DC.
72. Webster G, Embley T, Freitag T, Smith Z & Prosser J (2005) Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ Microbiol 7: 676-684.
73. West NE (1990) Structure and function of microphytic soil crusts in wildland ecosystems of arid to semi-arid regions. Adv Ecol Res 20: 179-223.
74. West NE (1991) Nutrient cycling in soils of semi-arid and arid regions. Semiarid Lands and Deserts: Soil Resource and Reclamation (Skujins j, ed.), pp. 295-332. M. Dekker, New York.
75. Yu J, Grishkan I & Steinberger Y (2012) Microfungal-community diversity in Zygophyllum dumosum and Hammada scoparia root zones in the northern Negev Desert. J Basic Microbiol 53: 390-400.
76. Zaady E (2005) Seasonal change and nitrogen cycling in a patchy Negev Desert: a review. Arid Land Res Manage 19: 111-124.
77. Zaady E, Groffman P & Shachak M (1998) Nitrogen fixation in macro- and microphytic patches in the Negev desert. Soil Biol Biochem 30: 449-454.
78. Zaady E, Ben-David EA, Sher Y, Tzirkin R & Nejidat A (2010) Inferring biological soil crust successional stage using combined PLFA, DGGE, physical and biophysiological analyses. Soil Biol Biochem 42: 842-849.
79. Zar JH (2010) Biostatistical Analysis. Pearson, Upper Saddle River, NJ.