Arbuscular mycorrhizal hyphae in grassland select for a diverse and abundant hyphospheric bacterial community involved in sulfonate desulfurization

Applied Soil Ecology

Volumn 89, Issue , 2015, Pages 113-121

  Gahan, Jacinta ^a   Schmalenberger, Achim ^a  

^a UNIVERSITY OF LIMERICK   (Ireland)

Author keywords

Arbuscular mycorrhiza; Bacterial community; Hyphosphere; Sulfur mobilization

Indexed keywords

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); FUNGI; GAMMAPROTEOBACTERIA;

EID: 84921867582     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2014.12.008     Document Type: Article

References (55)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
2. Andrade G., Mihara K.L., Linderman R.G., Bethlenfalvay G.J. Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi. Plant Soil 1997, 192:71-79.
3. Artursson V., Finlay R.D., Jansson J.K. Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ. Microbiol. 2006, 8:1-10.
4. Autry A.R., Fitzgerald J.W. Sulfonate S: a major form of forest soil organic sulfur. Biol. Fertil. Soils 1990, 10:50-56.
5. Bougoure D.S., Cairney J.W.G. Fungi associated with hair roots of Rhododendron lochiae (Ericaceae) in an Australian tropical cloud forest revealed by culturing and culture-independent molecular methods. Environ. Microbiol. 2005, 7:1743-1754.
6. Cornejo P., Azcón-Aguilar C., Miguel Barea J., Ferrol N. Temporal temperature gradient gel electrophoresis (TTGE) as a tool for the characterization of arbuscular mycorrhizal fungi. FEMS Microbiol. Lett. 2004, 241:265-270.
7. Faegri A., Torsvik V.L., Goksoyr J. Bacterial and fungal activities in soil: separation of bacteria and fungi by a rapid fractionated centrifugation technique. Soil Biol Biochem. 1977, 9:105-112.
8. Fox A., Kwapinski W., Griffiths B., Schmalenberger A. The role of sulfur and phosphorus mobilizing bacteria in biochar induced growth promotion of Lolium perenne. FEMS Microbiol. Ecol. 2014, 90:78-91.
9. Frey-Klett P., Garbaye J. Mycorrhiza helper bacteria: a promising model for the genomic analysis of fungal-bacterial interactions. New Phytol. 2005, 168:4-8.
10. Gardes M., Bruns T. ITS primers with enhanced specificity for Basidiomycetes: application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993, 2:113-118.
11. Graham J.H., Hodge N.C., Morton J.B. Fatty acid methyl ester profiles for characterization of Glomalean fungi and their endomycorrhizae. Appl. Environ. Microbiol. 1995, 61:58-64.
12. Gupta Sood S. Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. FEMS Microbiol. Ecol. 2003, 45:219-227.
13. Helgason T., Daniell T.J., Husband R., Fitter A.H., Young J.P.W. Ploughing up the wood-wide web?. Nature 1998, 394:431.
14. Heylen K., Vanparys B., Peirsegaele F., Lebbe L., De Vos P. Stenotrophomonas terrae sp. nov. and Stenotrophomonas humi sp. nov.: two nitrate-reducing bacteria isolated from soil. Int. J. Syst. Evol. Microbiol. 2007, 57:2056-2061.
15. Hodge A., Fitter A.H. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. PNAS 2010, 107:13754-13759.
16. Humphreys C.P., Franks P.J., Rees M., Bidartondo M.I., Leake J.R., Beerling D.J. Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat. Commun. 2010, 1:103.
17. Johansson J.F., Paul L.R., Finlay R.D. Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol. Ecol. 2004, 48:1-13.
18. Kaldorf M., Kuhn A., Schröder W., Hildebrandt U., Bothe H. Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J. Plant Physiol. 1999, 154:718-728.
19. Kertesz M.A., Mirleau P. The role of microbes in plant sulphur supply. J. Exp. Bot. 2004, 55:1939-1945.
20. Kertesz M.A., Fellows E., Schmalenberger A. Rhizobacteria and plant sulfur supply. Adv. Appl. Microbiol. 2007, 62:235-268.
21. Kowalchuk G.A., De Souza F.A., Van Veen J.A. Community analysis of arbuscular mycorrhizal fungi associated with Ammophila arenaria in Dutch coastal sand dunes. Mol. Ecol. 2002, 11:571-581.
22. Lane D.J. Nucleic Acid Techniques in Bacterial Systematics 1991, UK-$9. John Wiley & Sons, Chichester.
23. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar Buchner A., Lai T., Steppi S., Jobb G., Förster W., Brettske I., Gerber S., Ginhart A.W., Gross O., Grumann S., Hermann S., Jost R., König A., Liss T., Lüßmann R., May M., Nonhoff B., Reichel B., Strehlow R., Stamatakis A., Stuckmann N., Vilbig A., Lenke M., Ludwig T., Bode A., Schleifer K.H. ARB: a software environment for sequence data. Nucleic Acids Res. 2004, 32:1363-1371.
24. Mansfeld-Giese K., Larsen J., Bødker L. Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol. Ecol. 2002, 41:133-140.
25. McGrath S.P., Zhao F., Blake-Kalff M. History and Outlook for Sulphur Fertilizers in Europe 2003, International Fertilizer Society, York, UK.
26. Muyzer G., De Waal E., Uitterlindin A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59:695-700.
27. Reasoner D.J., Geldreich E.E. A new medium for the enumeration and subculture of bacteria from potable water. Appl. Environ. Microbiol. 1985, 49:1-7.
28. Roesch L.F., Fulthorpe R.R., Riva A., Casella G., Hadwin A.K., Kent A.D., Daroub S.H., Camargo F.A., Farmerie W.G., Triplett E.W. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 2007, 1:283-290.
29. Ruiz-Lozano J., Azcón R., Gomez M. Effects of arbuscular-mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl. Environ. Microbiol. 1995, 61:456-460.
30. Scheublin T.R., Sanders I.R., Keel C., van der Meer J.R. Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J. 2010, 4:752-763.
31. Schmalenberger A., Kertesz M.A. Desulfurization of aromatic sulfonates by rhizosphere bacteria: high diversity of the asfA gene. Environ. Microbiol. 2007, 9:535-545.
32. Schmalenberger A., Noll M. Shifts in desulfonating bacterial communities along a soil chronosequence in the forefield of a receding glacier. FEMS Microbiol. Ecol. 2010, 71:208-217.
33. Schmalenberger A., Schwieger F., Tebbe C.C. Effect of primers hybridizing to different evolutionarily conserved regions of the small-subunit rRNA gene in PCR-based microbial community analyses and genetic profiling. Appl. Environ. Microbiol. 2001, 67:3557-3563.
34. Schmalenberger A., Drake H.L., Kuesel K. High unique diversity of sulfate-reducing prokaryotes characterized in a depth gradient in an acidic fen. Environ. Microbiol. 2007, 9:1317-1328.
35. Schmalenberger A., Hodge S., Bryant A., Hawkesford M.J., Singh B.K., Kertesz M.A. The role of Variovorax and other Comamonadaceae in sulfur transformations by microbial wheat rhizosphere communities exposed to different sulfur fertilization regimes. Environ. Microbiol. 2008, 10:1486-1500.
36. Schmalenberger A., Telford A., Kertesz M.A. Sulfate treatment affects desulfonating bacterial community structures in Agrostis rhizospheres as revealed by functional gene analysis based on asfA. Eur. J. Soil Biol. 2010, 46:248-254.
37. Shaw R.K., Berger C.N., Feys B., Knutton S., Pallen M.J., Frankel G. Enterohemorrhagic Escherichia coli exploits EspA filaments for attachment to salad leaves. Appl. Environ. Microbiol. 2008, 74:2908-2914.
38. Simon L., Lalonde M., Bruns T. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl. Environ. Microbiol. 1992, 58:291-295.
39. Singh B.K., Millard P., Whiteley A.S., Murrell J.C. Unravelling rhizosphere-microbial interactions: opportunities and limitations. Trends Microbiol. 2004, 12:386-393.
40. Smith S.E., Read D.J. Mycorrhizal Symbiosis 2008, Academic Press, San Diego, CA.
41. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
42. Summerbell R.C. From Lamarckian fertilizers to fungal castles: recapturing the pre-1985 literature on endophytic and saprotrophic fungi associated with ectomycorrhizal root systems. Stud. Mycol. 2005, 53:191-256.
43. Tiunov A.V., Scheu S. Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia 2005, 142:636-642.
44. 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 Microbiol. Ecol. 2007, 61:295-304.
45. Toljander J.F., Santos-Gonzalez J.C., Tehler A., Finlay R.D. Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol. Ecol. 2008, 65:323-338.
46. Tommerup I. The role of mycorrhiza in plant populations and communities. Mycorrhiza 1992, 1:123-125.
47. Tunney H., Kirwan L., Fu W., Culleton N., Black A. Long-term phosphorus grassland experiment for beef production - impacts on soil phosphorus levels and liveweight gains. Soil Use Manage 2010, 26:237-244.
48. Vilariño A., Frey B., Shüepp H. MES [2-(N-morpholine)-ethane sulphonic acid] buffer promotes the growth of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices in an alkaline sand. Biol. Fertil. Soils 1997, 25:79-81.
49. Wagg C., Jansa J., Schmid B., van der Heijden M.G. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol. Lett. 2011, 14:1001-1009.
50. Warmink J.A., van Elsas J.D. Selection of bacterial populations in the mycosphere of Laccaria proxima: is type III secretion involved?. ISME J. 2008, 2:887-900.
51. Warmink J.A., Nazir R., Corten B., van Elsas J.D. Hitchhikers on the fungal highway: the helper effect for bacterial migration via fungal hyphae. Soil Biol. Biochem. 2011, 43:760-765.
52. White T.J., Bruns T., Lee S., Taylor J. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics 1990, Academic Press, San Diego, CA.
53. Wright S., Upadhyaya A. A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 1998, 198:97-107.
54. Xavier L.J., Germida J.J. Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol. Biochem. 2003, 35:471-478.
55. van der Heijden M.G.A., Bardgett R.D., van Straalen N.M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 2008, 11:296-310.