Direct and indirect influence of arbuscular mycorrhizal fungi on abundance and community structure of ammonia oxidizing bacteria and archaea in soil microcosms

Pedobiologia

Volumn 56, Issue 4-6, 2013, Pages 205-212

  Chen, Yong Liang ^a   Chen, Bao Dong ^a   Hu, Ya Jun ^a   Li, Tao ^a   Zhang, Xin ^a   Hao, Zhi Peng ^a   Wang, You Shan ^b  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b INSTITUTE OF PLANT AND ENVIRONMENT PROTECTION   (China)

Author keywords

Ammonia oxidizing archaea; Ammonia oxidizing bacteria; Arbuscular mycorrhizal fungi; Microbial community structure; Soil nitrogen cycling

Indexed keywords

ABUNDANCE; ALFALFA; AMMONIA; ARBUSCULAR MYCORRHIZA; BACTERIUM; COMMUNITY STRUCTURE; INOCULATION; MICROCOSM; NUTRIENT CYCLING; PLANT; POLYMERASE CHAIN REACTION;

ARBUSCULAR; ARCHAEA; BACTERIA (MICROORGANISMS); FUNGI; GLOMUS INTRARADICES; MEDICAGO SATIVA; NITROSOMONADALES;

EID: 84888003175     PISSN: 00314056     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pedobi.2013.07.003     Document Type: Article

References (52)

1. Amora-Lazcano E., Vázquez M.M., Azcón R. Response of nitrogen-transforming microorganisms to arbuscular mycorrhizal fungi. Biology and Fertility of Soils 1998, 27:65-70.
2. Avrahami S., Conrad R. Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Applied and Environmental Microbiology 2003, 69:6152-6164.
3. 2O release and on the community structure of ammonia oxidizers and denitrifiers. Applied and Environmental Microbiology 2002, 68:5685-5692.
4. Bollmann A., Bar-Gilissen M.J., Laanbroek H.J. Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Applied and Environmental Microbiology 2002, 68:4751-4757.
5. Cavagnaro T.R., Jackson L.E., Scow K.M., Hristova K.R. Effects of arbuscular mycorrhizas on ammonia oxidizing bacteria in an organic farm soil. Microbial Ecology 2007, 54:618-626.
6. Chen Y.L., Xu Z.W., Hu H.W., Hu Y.J., Hao Z.P., Jiang Y., Chen B.D. Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Applied Soil Ecology 2013, 68:36-45.
7. Di H.J., Cameron K.C., Shen J.P. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiology Ecology 2010, 72:386-394.
8. Fitter A.H., Stickland T.R., Harvey M.L., Wilson G.W. Architectural analysis of plant-root systems 1. Architectural correlates of exploitation efficiency. New Phytologist 1991, 118:375-382.
9. Francis C.A., Roberts K.J., Beman J.M., Santoro A.E., Oakley B.B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:14683-14688.
10. George E., Haussler K.U., Vetterlein D., Gorgus E., Marschner H. Water and nutrient translocation by hyphae of Glomus mosseae. Canadian Journal of Botany 1992, 70:2130-2137.
11. Giovannetti M., Mosse B. An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 1980, 84:489-500.
12. Gleeson D.B., MÜller C., Banerjee S., Ma W., Siciliano S.D., Murphy S.D. Response of ammonia oxidizing archea and bacteria to changing water filled pore space. Soil Biology and Biochemistry 2010, 42:1888-1891.
13. Hawkins H.J., Johansen A., George E. Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant and Soil 2000, 226:275-285.
14. He J.Z., Shen J.P., Zhang L.M., Zhu Y.G., Zheng Y.M., Xu M.G., Di H.J. 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. Environmental Microbiology 2007, 9:2364-2374.
15. Hodge A., Fitter A.H. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:13754-13759.
16. Hodge A., Campbell C.D., Fitter A.H. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 2001, 413:297-299.
17. Hooker J.E., Piatti P., Cheshire M.V., Watson C.A. Polysaccharides and monosaccharides in the hyphosphere of the arbuscular mycorrhizal fungi Glomus E3 and Glomus tenue. Soil Biology and Biochemistry 2007, 39:680-683.
18. 32P over defined distances. New Phytologist 1992, 120:509-516.
19. Jones D.L., Hodge A., Kuzyakov Y. Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 2004, 163:459-480.
20. Könneke M., Bernhard A.E., dela Torre J.R., Walker C.B., Waterbury J.B., Stahl D.A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437:543-546.
21. Kurola J., Salkinoja-Salonen M., Aarnio T., Hultman J., Romantschuk M. Activity, diversity and population size of ammonia-oxidising bacteria in oil-contaminated land farming soil. FEMS Microbiology Letters 2005, 250:33-38.
22. Leininger S., Urich T., Schloter M., Schwark L., Qi J., Nicol G.W. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 2006, 442:806-809.
23. Marschner P., Baumann K. Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant and Soil 2003, 251:279-289.
24. Marschner P., Timonen S. Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Applied Soil Ecology 2005, 28:23-36.
25. Martens-Habbena W., Stahl D.A. Nitrogen metabolism and kinetics of ammonia-oxidizing archaea. Methods in Enzymology 2011, 496:465-487.
26. Martens-Habbena W., Berube P.M., Urakawa H., de la Torre J.R., Stahl D.A. Ammonia oxidation kinetics determines niche separation of nitrifying Archaea and Bacteria. Nature 2009, 461:976-979.
27. Mendum T.A., Sockett R.E., Hirsch P.R. Use of molecular and isotopic techniques to monitor the response of autotrophic ammonia-oxidizing populations of the β subdivision of the class Proteobacteria in arable soils to nitrogen fertilizer. Applied Environmental Microbiology 1999, 65:4155-4162.
28. Newsham K.K., Fitter A.H., Watkinson A.R. Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. Journal of Ecology 1995, 83:991-1000.
29. Nicol G.W., Leininger S., Schleper C., Prosser J.I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology 2008, 10:2966-2978.
30. Olsen S.R., Cole C.V., Watanabe F.S., Dean L.A. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 1954, no. 939.
31. Pester M., Rattei T., Flechl S., Gröngröft A., Richter A., Overmann J., Reinhold-Hurek B., Loy A., Wagner M. amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environmental Microbiology 2012, 14:525-539.
32. Prosser J.I. The ecology of nitrifying bacteria. Biology of the Nitrogen Cycle 2007, 223-243. Elsevier, Amsterdam. H. Bothe, S.J. Ferguson, W.E. Newton (Eds.).
33. Reynolds H.L., Hartley A.E., Vogelsang K.M., Bever J.D., Schultz P.A. Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytologist 2005, 167:869-880.
34. Rillig M.C., Mummey D.L., Ramsey P.W., Klironomos J.N., Gannon J.E. Phylogeny of arbuscular mycorrhizal fungi predicts community composition of symbiosis-associated bacteria. FEMS Microbiology Ecology 2006, 57:389-395.
35. Rotthauwe J.H., Witzel K.P., Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology 1997, 63:4704-4712.
36. Santoro A.E., Francis C.A., De Sieyes N.R., Boehm A.B. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environmental Microbiology 2008, 10:1068-1079.
37. Scheublin T.R., Sanders I.R., Keel C., van de Meer J.R. Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. The ISME Journal 2010, 4:752-763.
38. Schüβler A., Schwarzott D., Walker C. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 2001, 105:1413-1421.
39. Shen J.P., Zhang L.M., Zhu Y.G., Zhang J.B., He J.Z. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environmental Microbiology 2008, 10:1601-1611.
40. Singh B.K., Numan N., Ridgway K.P., McNicol J., Young J.P.W., Daniell T.J., Prosser J.I., Millard P. Relationship between assemblages of mycorrhizal fungi and bacteria on grass roots. Environmental Microbiology 2008, 10:534-541.
41. Smith S.E., Read D.J. Mycorrhizal Symbiosis 2008, Academic Press. 2nd ed.
42. Tanaka Y., Yano K. Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant, Cell and Environment 2005, 28:1247-1254.
43. Toljander J.F., Lindahl B.D., Paul L.R., Elfstrand M., Finlay R.D. Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiology Ecology 2007, 61:295-304.
44. Tourna M., Stieglmeier M., Spang A., Könneke M., Schintlmeister A., Urich T., Engel M., Schloter M., Wagner M., Richter A., Schleper C. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings of the National Academy of Sciences of the United States of America 2011, 20:8420-8425.
45. Treusch A.H., Leininger S., Kletzin A., Schuster S.C., Klenk H.P., Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environmental Microbiology 2005, 7:1985-1995.
46. van der Heijden M.G.A., Engel R.S., Riedl R., Siegrist S. The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytologist 2006, 172:739-752.
47. Venter J.C., Remington K., Heidelberg J.F., Halpern A., Rusch D., Eisen J., Wu D., Paulsen I., Nelseon K., Nelson W., Fouts D., Levy S., Knap A., Lomas M., Nealson K., White O., Peterson J., Hoffman J., Parsons R., Tillson H.B., Pfannkoch C., Rogers Y., Smith H. Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004, 304:66-74.
48. Veresoglou S.D., Sen R., Mamolos A.P., Veresoglou D.S. Plant species identity and arbuscular mycorrhizal status modulate potential nitrification rates in nitrogen-limited grassland soils. Journal of Ecology 2011, 99:1339-1349.
49. Veresoglou S.D., Chen B.D., Rillig M.C. Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biology and Biochemistry 2012, 46:53-62.
50. Veresoglou S.D., Shaw L.J., Hooker J.E., Sen R. Arbuscular mycorrhizal modulation of diazotrophic and denitrifying microbial communities in the (mycor)rhizosphere of Plantago lanceolata. Soil Biology and Biochemistry 2012, 53:78-81.
51. Walker C.B., de la Torre J.R., Klotz M.G., Urakawa H., Pinela N., Arp D.J., Brochier-Armanet C., Chain P.S., Chan P.P., Gollabgir A., Hemp J., Hügler M., Karr E.A., Könneke M., Shin M., Lawton T.J., Lowe T., Martens-Habbena W., Sayavedra-Soto L.A., Lang D., Sievert S.M., Rosenzweig A.C., Manning G., Stahl D.A. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:8818-8823.
52. Yao Q., Wang L.R., Zhu H.H., Chen J.Z. Effect of arbuscular mycorrhizal fungal inoculation on root system architecture of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Scientia Horticulturae 2009, 121:458-461.