Impact of land use on arbuscular mycorrhizal fungal communities in rural Canada

Applied and Environmental Microbiology

Volumn 79, Issue 21, 2013, Pages 6719-6729

  Dai, Mulan ^a   Bainard, Luke D ^a   Hamel, Chantal ^a   Gan, Yantai ^a   Lynch, Derek ^b  

^a SWIFT CURRENT RESEARCH AND DEVELOPMENT CENTRE   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LAND USE; RNA; ROADSIDES;

ARBUSCULAR MYCORRHIZAL; ARBUSCULAR MYCORRHIZAL FUNGI; CROPLAND MANAGEMENT; DIFFERENT LAND USE TYPES; DIFFERENT STRUCTURE; FUNGAL COMMUNITY; HIGHLY-CORRELATED; STRUCTURAL SHIFTS;

FUNGI;

ECOZONE; FUNGUS; HABITAT CONSERVATION; LAND USE; PRAIRIE; RNA; RURAL AREA; SAMPLING; SOIL MICROORGANISM; SPECIES RICHNESS;

CANADA;

ARBUSCULAR; FUNGI; GLOMERACEAE; GLOMEROMYCOTA; TRITICUM AESTIVUM;

RNA 18S;

AGRICULTURE; ANALYSIS OF VARIANCE; ARTICLE; BIODIVERSITY; CANADA; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ENVIRONMENTAL PROTECTION; GENETICS; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MOLECULAR GENETICS; MYCORRHIZA; NUCLEOTIDE SEQUENCE; PHYLOGENY; SOIL; WHEAT;

AGRICULTURE; ANALYSIS OF VARIANCE; BASE SEQUENCE; BIODIVERSITY; CANADA; CONSERVATION OF NATURAL RESOURCES; GEOGRAPHY; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; PHYLOGENY; RNA, RIBOSOMAL, 18S; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY; TRITICUM;

EID: 84886885341     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01333-13     Document Type: Article

References (84)

1. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D. 2010. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519-530.
2. Fitter AH, Helgason T, Hodge A. 2011. Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biol. Rev. 25:68-72.
3. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. Academic Press, New York, NY.
4. Doubková P, Suda J, Sudová R. 2012. The symbiosis with arbuscular mycorrhizal fungi contributes to plant tolerance to serpentine edaphic stress. Soil Biol. Biochem. 44:56-64.
5. Hawkins HJ, Johansen A, George E. 2000. Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275-285.
6. Smith SE, Facelli E, Pope S, Smith FA. 2010. Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3-20.
7. van der Heijden MGA. 2010. Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 91:1163-1171.
8. Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW. 2012. Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169:895-904.
9. Ruth B, Khalvati M, Schmidhalter U. 2011. Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant Soil 342:459-468.
10. Garg N, Chandel S. 2011. Effect of mycorrhizal inoculation on growth, nitrogen fixation, and nutrient uptake in Cicer arietinum L. under salt stress. Turk. J. Agr. For. 35:205-214.
11. Rillig MC, Mummey DL. 2006. Mycorrhizas and soil structure. New Phytol. 171:41-53.
12. Gosling P, Hodge A, Goodlass G, Bending GD. 2006. Arbuscular mycorrhizal fungi and organic farming. Agric. Ecosyst. Environ. 113:17-35.
13. Kahiluoto H, Vestberg M. 1998. The effect of arbuscular mycorrhiza on biomass production and phosphorus uptake from sparingly soluble sources by leek (Allium porrum L.) in Finnish field soils. Biol. Agric. Hortic. 16:65-85.
14. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880-882.
15. An ZQ, Hendrix JW, Hershman DE, Ferriss RS, Henson GT. 1993. The influence of crop rotation and soil fumigation on a mycorrhizal fungal community associated with soybean. Mycorrhiza 3:171-182.
16. Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A. 2003. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl. Environ. Microbiol. 69:2816-2824.
17. Fester T, Sawers R. 2011. Progress and challenges in agricultural applications of arbuscular mycorrhizal fungi. Crit. Rev. Plant Sci. 30:459-470.
18. Anderson EL, Millner PD, Kunishi HM. 1987. Maize root length density and mycorrhizal infection as influenced by tillage and soil phosphorus. J. Plant Nutr. 10:1349-1356.
19. Jakobsen I, Nielsen NE. 1983. Vesicular-arbuscular mycorrhiza in fieldgrown crops. I. Mycorrhizal infection in cereals and peas at various times and soil depths. New Phytol. 93:401-413.
20. Santos-González JC, Nallanchakravarthula S, Alström S, Finlay RD. 2011. Soil, but not cultivar, shapes the structure of arbuscular mycorrhizal fungal assemblages associated with strawberry. Microb. Ecol. 62:25-35.
21. Wang FY, Tong RJ, Shi Zy Xu XF, He XH. 2011. Inoculations with arbuscular mycorrhizal fungi increase vegetable yields and decrease phoxim concentrations in carrot and green onion and their soils. PLoS One 6(2):e16949. doi:10.11371/journal.pone.0016949.
22. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW. 1998. Ploughing up the wood-wide web? Nature 394:431. doi:10.1038/28764.
23. Hijri I, Sỳkorová Z, Oehl F, Ineichen K, Mäder P, Wiemken A, Redecker D. 2006. Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol. Ecol. 15:2277-2289.
24. Verbruggen E, Van Der Heijden MGA, Weedon JT, Kowalchuk GA, Rö-Ling WFM. 2012. Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol. Ecol. 21: 2341-2353.
25. Huffman T, Eilers W. 2011. Farm land management. 4. Agricultural land use. In Environmental sustainability of Canadian agriculture: agrienvironmental indicator report series, report no. 3. Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada. http://publications.gc.ca/si te/archivee-archived.html?url,http://publications.gc.ca/collections/coll ection_2011/agr/A22-201-2010-eng.pdf.
26. Ecological Stratification Working Group. 1996. A national ecological framework for Canada. Minister of Supply and Services Canada, Ottawa, Ontario, Canada. http://sis.agr.gc.ca/cansis/publications/ecostrat/cad _report.pdf.
27. Soil Classification Working Group. 1998. The Canadian system of soil classification, 3rd ed. Agriculture and Agri-Food Canada Publication 1646 NRC Research Press, Ottawa, ON, Canada. http://sis.agr.gc.ca /cansis/publications/manuals/1998-cssc-ed3/cssc3_manual.pdf.
28. Campbell CA, Zentner RP, Janzen HH, Bowren KE. 1990. Crop rotation studies on the Canadian prairies. Research Branch, Agriculture Canada publication 1841/E. Research Branch, Agriculture Canada, Ottawa, ON, Canada.
29. Roche. 2009. Technical bulletin. Genome sequencer FLX system. Amplicon fusion primer design guidelines for GS FLX titanium series Lib-A chemistry. TCB no. 013-2009. Roche, Basel, Switzerland. http://www.igsb .org/uploads/pdf/TCB-09013_AmpliconFusionPrimerDesignGuidelines. pdf.
30. Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V. 2010. Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ. Microbiol. 12:2165-2179.
31. Sato K, Suyama Y, Saito M, Sugawara K. 2005. A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Jpn. Soc. Grassl. Sci. 51: 179-181.
32. Polz MF, Cavanaugh CM. 1998. Bias in template-to-product ratios in multitemplate PCR. Appl. Environ. Microbiol. 64:3724-3730.
33. Huse SM, Welch DM, Morrison HG, Sogin ML. 2010. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ. Microbiol. 12:1889-1898.
34. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
35. Edgar RC. 2004. MUSCLE: multiple sequence alignment with improved accuracy and speed, p 728-729. In . Proceedings of the 2004 IEEE Computational Systems Bioinformatics Conference (CSB 2004). The IEEE Computer Society, Washington, DC. doi:10.1109/CSB.2004.1332560.
36. Zhang Z, Schwartz S, Wagner L, Miller W. 2000. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 7:203-214.
37. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
38. 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. 28:2731-2739.
39. Hall BG. 2004. Phylogenetic trees made easy. A how-to manual. Sinauer Associates, Sunderland, MA.
40. Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C. 2013. An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza doi:10.1007/s00572 -013-0486-y.
41. Peck JE. 2010. Multivariate analysis for community ecologists: step-bystep using PC-ORD. MjM Software Design, Gleneden Beach, OR.
42. de Mendiburu F. 2013. Statistical procedures for agricultural research. Package 'Agricolae,' version 1.4-4. Comprehensive R Archive Network, Institute for Statistics and Mathematics, Vienna, Austria. http://cran.r -project.org/web/packages/agricolae/agricolae.pdf.
43. McCune B, Grace JB. 2002. Analysis of ecological communities. MjM Software Design, Gleneden Beach, OR.
44. Legendre P, Legendre L. 1998. Numerical ecology. Elsevier, Amsterdam, Netherlands.
45. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B. 2013. Various R programming tools for plotting data. Package 'gplots,' version 211.3. Comprehensive R Archive Network, Institute for Statistics and Mathematics, Vienna, Austria. http://cran.r-project.org/web/packages/gplots /gplots.pdf.
46. Neuwirth E. 2011. ColorBrewer palettes. Package 'RColorBrewer,' version 10-5. Comprehensive R Archive Network, Institute for Statistics and Mathematics, Vienna, Austria. http://cran.r-project.org/web/packages /RColorBrewer/RColorBrewer.pdf
47. Postma-Blaauw MB. 2010. Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91: 460-473.
48. Andersen R, Chapman SJ, Artz RRE. 2013. Microbial communities in natural and disturbed peatlands: a review. Soil Biol. Biochem. 57:979-994.
49. Richardson PJ, MacDougall AS, Larson DW. 2012. Fine-scale spatial heterogeneity and incoming seed diversity additively determine plant establishment. J. Ecol. 100:939-949.
50. Hamel C, Schellenberg MP, Hanson K, Wang H. 2007. Evaluation of the "bait-lamina test" to assess soil microfauna feeding activity in mixed grassland. Appl. Soil Ecol. 36:199-204.
51. Jansa J, Wiemken A, Frossard E. 2006. The effects of agricultural practices on arbuscular mycorrhizal fungi. Geol. Soc. Lond. Spec. Publ. 266: 89-115. doi:10.1144/GSL.SP.2006.266.01.01.
52. Douds DD, Jr, Millner PD. 1999. Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agric. Ecosyst. Environ. 74:77-93.
53. Jansa J, Mozafar A, Banke S, McDonald BA, Frossard E. 2002. Intra-and intersporal diversity of ITS rDNA sequences in Glomus intraradices assessed by cloning and sequencing, and by SSCP analysis. Mycol. Res. 106:670-681.
54. Jumpponen A, Trowbridge J, Mandyam K, Johnson L. 2005. Nitrogen enrichment causes minimal changes in arbuscular mycorrhizal colonization but shifts community composition-evidence from rDNA data. Biol. Fertil. Soils 41:217. doi:10.1007/s00374-005-0845-8.
55. Oehl F, Sieverding E, Mäder P, Dubois D, Ineichen K, Boller T, Wiemken A. 2004. Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574-583.
56. Dodd J, Boddington C, Rodriguez A, Gonzalez-Chavez C, Mansur I. 2000. Mycelium of arbuscular mycorrhizal fungi (AMF) from different genera: form, function and detection. Plant Soil 226:131-151.
57. Schnoor TK, Lekberg Y, Rosendahl S, Olsson PA. 2011. Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21:211-220.
58. Alguacil MM, Lumini E, Roldàn A, Salinas-Garcia JR, Bonfante P, Bianciotto V. 2008. The impact of tillage practices on arbuscular mycorrhizal fungal diversity in subtropical crops. Ecol. Appl. 18:527-536.
59. Brito I, Goss MJ, de Carvalho M, Chatagnier O, van Tuinen D. 2012. Impact of tillage system on arbuscular mycorrhiza fungal communities in the soil under Mediterranean conditions. Soil Till. Res. 121:63-67.
60. Schnoor TK, Mårtensson LM, Olsson PA. 2011. Soil disturbance alters plant community composition and decreases mycorrhizal carbon allocation in a sandy grassland. Oecologia 167:809-819. doi:10.1007/s00442-011-2020-2.
61. Grevers MC, Kirkland JA, De Jong E, Rennie DA. 1986. Soil water conservation under zero-and conventional tillage systems on the Canadian prairies. Soil Till. Res. 8:265-276.
62. Lafond GP, May WE, Stevenson FC, Derksen DA. 2006. Effects of tillage systems and rotations on crop production for a thin Black Chernozem in the Canadian Prairies. Soil Till. Res. 89:232-245.
63. Campbell CA, Read DWL, Zentner RP, Leyshon AJ, Ferguson WS. 1983. First 12 years of a long-term crop rotation study in southwestern Saskatchewan-yields and quality of grain. Can. J. Plant Sci. 63:91-108.
64. Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E. 2010. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol. Biochem. 42:724-738.
65. Oehl F, Sieverding E, Ineichen K, Mäder P, Wiemken A, Boller T. 2009. Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agric. Ecosyst. Environ. 134:257-268.
66. Gosling P, Ozaki A, Jones J, Turner M, Rayns F, Bending GD. 2010. Organic management of tilled agricultural soils results in a rapid increase in colonisation potential and spore populations of arbuscular mycorrhizal fungi. Agric. Ecosyst. Environ. 139:273-279.
67. Koide RT. 1991. Tansley review no. 29. Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol. 117:365-386.
68. Lakshmipathy A, Gowda B, Bagyaraj DJ. 2003. VA mycorrhizal colonization pattern in RET medicinal plants (Mammea suriga, Saraca asoca, Garcinia spp., Embelia ribes and Calamus sp.) in different parts of Karnataka. Asian J. Microbiol. Biotechnol. Environ. Sci. 5:505-508.
69. Lakshmipathy R, Balakrishna AN, Bagyaraj DJ. 2012. Abundance and diversity of AM fungi across a gradient of land use intensity and their seasonal variations in Niligiri Biosphere of the Western Ghats, India. J. Agric. Sci. Technol. 14:903.
70. Van Aarle IM, Plassard C. 2010. Spatial distribution of phosphatase activity associated with ectomycorrhizal plants is related to soil type. Soil Biol. Biochem. 42:324-330.
71. Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A. 2006. The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol. Lett. 9:501-515.
72. Avio L, Cristani CC, Strani P, Giovannetti M. 2009. Genetic and phenotypic diversity of geographically different isolates of Glomus mosseae. Can. J. Microbiol. 55:242-253.
73. Rosendahl S, McGee P, Morton JB. 2009. Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol. Ecol. 18:4316-4329.
74. Talukdar NC, Germida JJ. 1993. Occurrence and isolation of vesiculararbuscular mycorrhizae in cropped field soils of Saskatchewan, Canada. Can. J. Microbiol. 39:567-575.
75. Egerton-Warburton LM, Johnson NC, Allen EB. 2007. Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecol. Monogr. 77:527-544.
76. Fitzsimons MS, Miller RM, Jastrow JD. 2008. Scale-dependent niche axes of arbuscular mycorrhizal fungi. Oecologia 158:117-127.
77. Johnson NC, Tilman D, Wedin D. 1992. Plant and soil controls on mycorrhizal fungal communities. Ecology 73:2034-2042.
78. Al-Yahya'ei MN, Oehl F, Vallino M, Lumini E, Redecker D, Wiemken A, Bonfante P. 2011. Unique arbuscular mycorrhizal fungal communities uncovered in date palm plantations and surrounding desert habitats of southern Arabia. Mycorrhiza 21:195-209.
79. Yang C, Hamel C, Schellenberg MP, Perez JC, Berbara RL. 2010. Diversity and functionality of arbuscular mycorrhizal fungi in three plant communities in semiarid Grasslands National Park, Canada. Microb. Ecol. 59:724-733.
80. Curtis BC, Rajaram S, Macpherson HG (ed). 2002. Wheat in the world. Bread wheat improvement and production. FAO, Rome, Italy. http: //www.fao.org/docrep/006/Y4011E/Y4011E00.HTM.
81. Dai M, Hamel C, St Arnaud M, He Y, Grant C, Lupwayi N, Janzen H, Malhi S S, Yang X, Zhou Z. 2012. Arbuscular mycorrhizal fungi assemblages in Chernozem great groups revealed by massively parallel pyrosequencing. Can. J. Microbiol. 58:81-92.
82. Blaszkowski J, Kovács GM, Balázs TK, Orlowska E, Sadravi M, Wubet T, Buscot F. 2010. Glomus africanum and G. iranicum, two new species of arbuscular mycorrhizal fungi (Glomeromycota). Mycologia 102:1450-1462.
83. Ellouze W, Hamel C, Vujanovic V, Gan YT, Bouzid S, St-Arnaud M. 2013. Chickpea genotypes shape the soil microbiome and affect the establishment of the subsequent durum wheat crop in the semiarid North American Great Plains. Soil Biol. Biochem. 63:129-141.
84. Ma WK, Siciliano SD, Germida JJ. 2005. A PCR-DGGE method for detecting arbuscular mycorrhizal fungi in cultivated soils. Soil Biol. Biochem. 37:1589-1597.