Ectomycorrhizal roots select distinctive bacterial and ascomycete communities in Swedish subarctic forests

Environmental Microbiology

Volumn 13, Issue 3, 2011, Pages 819-830

  Izumi, Hironari ^a   Finlay, Roger D ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASCOMYCETES; BACTERIUM; BIRCH; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MYCORRHIZA; POLYMERASE CHAIN REACTION; SWEDEN; TREE;

ASCOMYCOTA; BACTERIA; BETULA; MYCORRHIZAE; POLYMERASE CHAIN REACTION; SOIL MICROBIOLOGY; SWEDEN; TREES;

ASCOMYCOTA; BACTERIA (MICROORGANISMS); BETULA PUBESCENS; FUNGI; LACTARIUS; LACTARIUS TORMINOSUS; LECCINUM VARIICOLOR; PILODERMA FALLAX; PSEUDOTOMENTELLA; PSEUDOTOMENTELLA TRISTIS; TOMENTELLOPSIS SUBMOLLIS;

EID: 79952093658     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02393.x     Document Type: Article

References (71)

1. Agerer, R. (1987) Colour Atlas of Ectomycorrhizae. Munich, Germany: Einhorn-Verlag.
2. Artursson, V., and Jansson, J.K. (2003) Use of bromodeoxyuridine immunocapture to identify active bacteria associated with arbuscular mycorrhizal hyphae. Appl Environ Microbiol 69: 6208-6215.
3. den Bakker, H.C., Gravendeel, B., and Kuyper, T.W. (2004) An ITS phylogeny of Leccinum and an analysis of the evolution of minisatellite-like sequences within ITS1. Mycologia 96: 102-118.
4. Bending, G.D., Poole, E.J., Whipps, J.M., and Read, D.J. (2002) Characterisation of bacteria from Pinus sylvestris-Suillus luteus mycorrhizas and their effects on root-fungus interactions and plant growth. FEMS Microbiol Ecol 39: 219-227.
5. Bertaux, J., Schmid, M., Hutzler, P., Hartmann, A., Garbaye, J., and Frey-Klett, P. (2005) Occurrence and distribution of endobacteria in the plant-associated mycelium of the ECM fungus Laccaria bicolor S238N. Environ Microbiol 7: 1786-1795.
6. Bianciotto, V., Lumini, E., Lanfranco, L., Minerdi, D., Bonfante, P., and Perottos, S. (2000) Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae. Appl Environ Microbiol 66: 4503-4509.
7. de Boer, W., Folman, L.B., Summerbell, R.C., and Boddy, L. (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29: 795-811.
8. Boersma, F.G.H., Warmink, J.A., Andreote, F.A., and van Elsas, J.D. (2009) Selection of Sphingomonadaceae at the base of Laccaria proxima and Russula exalbicans fruiting bodies. Appl Environ Microbiol 75: 1979-1989.
9. Bonfante, P., and Anca, I.-A. (2009) Plants, mycorrhizal fungi and bacteria: a network of interactions. Annu Rev Microbiol 63: 363-383.
10. Bruns, T.D., Szaro, T.M., Gardes, M., Cullings, K.W., Pan, J.J., Taylor, D.L., etal. (1998) A sequence database for the identification of ECM basidiomycetes by phylogenetic analysis. Mol Ecol 7: 257-272.
11. Budi, S.W., van Tuinen, D., Martinotti, G., and Gianinazzi, S. (1999) Isolation from the Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soilborne fungal pathogens. Appl Environ Microbiol 65: 5148-5150.
12. Burke, D.J., Dunham, S.M., and Kretzer, A.M. (2008) Molecular analysis of bacterial communities associated with the roots of Douglas fir (Pseudotsuga menziesii) colonized by different ECM fungi. FEMS Microbiol Ecol 65: 299-309.
13. Clemmensen, K.E., and Michelsen, A. (2006) Integrated long-term responses of an arctic-alpine willow and associated ECM fungi to an altered environment. Can J Bot 84: 831-843.
14. Cripps, C.L., and Eddington, L.H. (2005) Distribution of mycorrhizal types among alpine vascular plant families on the Beartooth Plateau, rocky mountains, USA, in reference to large-scale patterns in arctic-alpine habitats. Arct Antarct Alp Res 37: 177-188.
15. Frey-Klett, P., Garbaye, J., and Tarkka, M. (2007) The mycorrhiza helper bacteria revisited. New Phytol 176: 22-36.
16. Frey, P., Frey-Klett, P., Garbaye, J., Berge, O., and Heulin, T. (1997) Metabolic and Genotypic Fingerprinting of Fluorescent Pseudomonads Associated with the Douglas Fir-Laccaria bicolor Mycorrhizosphere. Appl Environ Microbiol 63: 1852-1860.
17. Frey-Klett, P., Chavatte, M., Clausse, M.L., Courrier, S., Le Roux, C., Raaijmakers, J., etal. (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonad. New Phytol 165: 317-328.
18. Gardes, M., and Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113-118.
19. Grelet, G.A., Johnson, D., Paterson, E., Anderson, I.C., and Alexander, I.J. (2009) Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New Phytol 182: 359-366.
20. Grelet, G.A., Johnson, D., Vrålstad, T., Alexander, I.J., and Anderson, I.C. (2010) New insights into the mycorrhizal Rhizoscyphus ericae aggregate: spatial structure and co-colonization of ECM and ericoid roots. New Phytol 188: 210-222.
21. Heinonsalo, J., Koskiahde, I., and Sen, R. (2007) Scots pine bait seedling performance and root colonizing ECM fungal community dynamics before and during the 4 years after forest clear-cut logging. Can J For Res 37: 415-429.
22. Höppener-Ogawa, S., Leveau, J.H.J., Hundscheid, M.P.J., Van Veen, J.A., and De Boer, W. (2009) Impact of Collimonas bacteria on community composition of soil fungi. Environ Microbiol 11: 1444-1452.
23. Hrynkiewicz, K., Baum, C., and Leinweber, P. (2009) Mycorrhizal community structure, microbial biomass P and phosphatase activities under Salix polaris as influenced by nutrient availability. Eur J Soil Biol 45: 168-175.
24. Izumi, H., Anderson, I.C., Alexander, I.J., Killham, K., and Moore, E.R.B. (2006a) Diversity and expression of nitrogenase genes (nifH) from ectomycorrhizas of Corsican pine (Pinus nigra). Environ Microbiol 8: 2224-2230.
25. Izumi, H., Anderson, I.C., Alexander, I.J., Killham, K., and Moore, E.R.B. (2006b) Endobacteria in some ectomycorrhiza of Scots pine (Pinus sylvestris). FEMS Microbiol Ecol 56: 34-43.
26. Izumi, H., Moore, E.R.B., Killham, K., Alexander, I.J., and Anderson, I.C. (2007) Characterisation of endobacterial communities in ectomycorrhizas by DNA- and RNA-based molecular methods. Soil Biol Biochem 39: 891-899.
27. Jonasson, S., and Michelsen, A. (1996) Nutrient cycling in subarctic and arctic ecosystems, with special reference to the Abisko and Torneträsk region. Ecol Bull 45: 45-52.
28. Kataoka, R., Taniguchi, T., Ooshima, H., and Futai, K. (2008) Comparison of the bacterial communities established on the mycorrhizae formed on Pinus thunbergii root tips by eight species of fungi. Plant Soil 304: 267-275.
29. Kataoka, R., Taniguchi, T., and Futai, K. (2009) Fungal selectivity of two mycorrhiza helper bacteria on five mycorrhizal fungi associated with Pinus thunbergii. World J Microbiol Biotechnol 25: 1815-1819.
30. King, J.S., Albaugh, T.J., Allen, H.L., Buford, M., Strain, B.R., and Dougherty, P. (2002) Below-ground carbon input to soil is control led by nutrient availability and fine root dynamics in loblolly pine. New Phytol 154: 389-398.
31. Kjøller, R., Olsrud, M., and Michelsen, A. (2010) Co-existing ericaceous plant species in a subarctic mire community share fungal root endophytes. Fun Ecol 3: 205-214.
32. Klappenbach, J.A., Dunbar, J.M., and Schmidt, T.M. (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66: 1328-1333.
33. Koljalg, U., Larsson, K.H., Abarenkov, K., Nilsson, R.H., Alexander, I.J., Eberhardt, U., etal. (2005) UNITE: a database providing web-based methods for the molecular identification of ECM fungi. New Phytol 166: 1063-1068.
34. Larena, I., Salazar, O., Gonzalez, V., Julian, M.C., and Rubio, V. (1999) Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. J Biotechnol 75: 187-194.
35. Leake, J.R., Johnson, D., Donnelly, D.P., Muckle, G.E., Boddy, L., and Read, D.J. (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82: 1016-1045.
36. Li, C.Y., Massicotte, H.B., and Moore, L.V.H. (1992) Nitrogen-fixing Bacillus sp. associated with Douglas-fir tuberculate ectomycorrihzae. Plant Soil 140: 35-40.
37. Lindahl, B.D., Ihrmark, K., Boberg, J., Trumbore, S.E., Hogberg, P., Stenlid, J., and Finlay, R.D. (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173: 611-620.
38. Lindahl, B.D., de Boer, W., and Finlay, R.D. (2010) Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi. ISME J 4: 872-881.
39. McCune, B., and Grace, J.B. (2002) Analysis of Ecological Communities. Gleneden Beach, OR, USA: MjM Software design.
40. Mandyam, K., and Jumpponen, A. (2005) Seeking the elusive function of the root-colonising dark septate endophyte. Stud Mycol 53: 173-189.
41. Mogge, B., Loferer, C., Agerer, R., Hutzler, P., and Hartmann, A. (2000) Bacterial community structure and colonization patterns of Fagus sylvatical-ectomycorrhizospheres as determined by fluorescence in situ hybridization and confocal laser scanning microscopy. Mycorrhiza 9: 271-278.
42. Muyzer, G., Dewaal, E.C., and Uitterlinden, A.G. (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes-coding for 16s ribosomal RNA. Appl Environ Microbiol 59: 695-700.
43. Naumann, M., Schüssler, A., and Bonfante, P. (2010) The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME J 4: 862-871.
44. Nurmiaho-Lassila, E.L., Timonen, S., Haahtela, K., and Sen, R. (1997) Bacterial colonization patterns of intact Pinus sylvestris mycorrhizospheres in dry pine forest soil: an electron microscopy study. Can J Microbiol 43: 1017-1035.
45. Ohara, H., and Hamada, M. (1967) Disappearance of bacteria from the zone of active mycorrhizas in Tricoloma matsutake (S. Ito et Imai) Singer. Nature 213: 528-529.
46. Olsson, P.A., Chalot, M., Baath, E., Finlay, R.D., and Soderstrom, B. (1996) ECM mycelia reduce bacterial activity in a sandy soil. FEMS Microbiol Ecol 21: 77-86.
47. Partida-Martinez, L.P., and Hertweck, C. (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437: 884-888.
48. Paul, L.R., Chapman, B.K., and Chanway, C.P. (2007) Nitrogen fixation associated with Suillus tomentosus tuberculate ectomycorrhizae on Pinus contorta ver. latifolia. Ann Bot 99: 1101-1109.
49. Poole, E.J., Bending, G.D., Whipps, J.M., and Read, D.J. (2001) Bacteria associated with Pinus sylvestris-Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro. New Phytol 151: 743-751.
50. Rosling, A., Landeweert, R., Lindahl, B.D., Larsson, K.-H., Kuyper, T.W., Taylor, A.F.S., and Finlay, R.D. (2003) Vertical distribution of ectomycorrhizal taxa in a podzol soil profile. New Phytol 159: 775-783.
51. Rousk, J., Demoling, L.A., Bahr, A., and Bååth, E. (2008) Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol Ecol 63: 350-358.
52. Salvioli, A., Chiapello, M., Fontaine, J., Hadj-Sahraoui, A.L., Grandmougin-Ferjani, A., Lanfranco, L., and Bonfante, P. (2010) Endobacteria affect the metabolic profile of their host Gigaspora margarita, an arbuscular mycorrhizal fungus. Environ Microbiol 12: 2083-2095.
53. Scheublin, T.R., Sanders, I.R., Keel, C., and van der Meer, J.R. (2010) Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J 4: 752-763.
54. Sen, R. (2000) Budgeting for the wood-wide web. New Phytol 145: 161-163.
55. Sonesson, M., and Lundberg, B. (1974) Late quaternary forest development of the Torneträsk area, north Sweden. Oikos 25: 121-133.
56. Sun, Y.P., Unestam, T., Lucas, S.D., Johanson, K.L., Kenne, L., and Finlay, R. (1999) Exudation-reabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and soil microorganisms. Mycorrhiza 9: 137-144.
57. Taylor, A.F.S., and Alexander, I. (2005) The ECM symbiosis in the real world. Mycologist 19: 102-112.
58. Tedersoo, L., Suvi, T., Larsson, E., and Kõljalg, U. (2006) Diversity and community structure of ectomycorrhizal fungi in a wooded meadow. Mycol Res 110: 734-748.
59. Tedersoo, L., Partel, K., Jairus, T., Gates, G., Poldmaa, K., and Tamm, H. (2009) Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. Environ Microbiol 12: 3166-3178.
60. Timonen, S., Jorgensen, K.S., Haahtela, K., and Sen, R. (1998) Bacterial community structure at defined locations of Pinus sylvestris-Suillus bovinus and Pinus sylvestris-Paxillus involutus mycorrhizospheres in dry pine forest humus and nursery peat. Can J Microbiol 44: 499-513.
61. Toljander, J.F., Artursson, V., Paul, L.R., Jansson, J.K., and Finlay, R.D. (2006) Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett 254: 34-40.
62. Toljander, J.F., Paul, L., Lindahl, B.D., Elfstrand, M., and Finlay, R.D. (2007) Influence of AM fungal exudates on bacterial community structure. FEMS Microbiol Ecol 61: 295-304.
63. Tornberg, K., Baath, E., and Olsson, S. (2003) Fungal growth and effects of different wood decomposing fungi on the indigenous bacterial community of polluted and unpolluted soils. Biol Fertil Soils 37: 190-197.
64. Urban, A., Puschenreiter, M., Strauss, J., and Gorfer, M. (2008) Diversity and structure of ECM and co-associated fungal communities in a serpentine soil. Mycorrhiza 18: 339-354.
65. Uroz, S., Calvaruso, C., Turpault, M.-P., and Frey-Klett, P. (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17: 378-387.
66. Uroz, S., Buee, M., Murat, C., Frey-Klett, P., and Martin, F. (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microbiol Rep 2: 281-288.
67. Vandenkoornhuyse, P., Mahe, S., Ineson, P., Staddon, P., Ostle, N., Cliquet, J.B., etal. (2007) Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proc Natl Acad Sci USA 104: 16970-16975.
68. Vrålstad, T., Myhre, E., and Schumacher, T. (2002) Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the Helotiales in burnt and metal polluted habitats. New Phytol 155: 131-148.
69. Wallander, H., Nilsson, L.O., Hagerberg, D., and Baath, E. (2001) Estimation of the biomass and seasonal growth ofexternal mycelium of ECM fungi in the field. New Phytol 151: 753-760.
70. Warmink, J.A., Nazir, R., and van Elsas, J.D. (2009) Universal and species-specific bacterial 'fungiphiles' in the mycospheres of different basidiomycetous fungi. Environ Microbiol 11: 300-312.
71. Wu, B., Nara, K., and Hogetsu, T. (2005) Genetic structure of Cenococcum geophilum populations in primary successional volcanic deserts on Mount Fuji as revealed by microsatellite markers. New Phytol 165: 285-293.