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Functional Profiling and Distribution of the Forest Soil Bacterial Communities Along the Soil Mycorrhizosphere Continuum

  • Soil Microbiology
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Abstract

An ectomycorrhiza is a multitrophic association between a tree root, an ectomycorrhizal fungus, free-living fungi and the associated bacterial communities. Enzymatic activities of ectomycorrhizal root tips are therefore result of the contribution from different partners of the symbiotic organ. However, the functional potential of the fungus-associated bacterial communities remains unknown. In this study, a collection of 80 bacterial strains randomly selected and isolated from a soil–ectomycorrhiza continuum (oak–Scleroderma citrinum ectomycorrhizas, the ectomycorrhizosphere and the surrounding bulk soil) were characterized. All the bacterial isolates were identified by partial 16S rRNA gene sequences as members of the genera Burkholderia, Collimonas, Dyella, Mesorhizobium, Pseudomonas, Rhizobium and Sphingomonas. The bacterial strains were then assayed for β-xylosidase, β-glucosidase, N-acetyl-hexosaminidase, β-glucuronidase, cellobiohydrolase, phosphomonoesterase, leucine-aminopeptidase and laccase activities, chitin solubilization and auxin production. Using these bioassays, we demonstrated significant differences in the functional distribution of the bacterial communities living in the different compartments of the soil–ectomycorrhiza continuum. The surrounding bulk soil was significantly enriched in bacterial isolates capable of hydrolysing cellobiose and N-acetylglucosamine. In contrast, the ectomycorrhizosphere appeared significantly enriched in bacterial isolates capable of hydrolysing glucopyranoside and chitin. Notably, chitinase and laccase activities were found only in bacterial isolates belonging to the Collimonas and Pseudomonas genera. Overall, the results suggest that the ectomycorrhizal fungi favour specific bacterial communities with contrasting functional characteristics from the surrounding soil.

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References

  1. Agerer R (2001) Exploration types of ectomycorrhizae: a proposal to classify ectomycorrhizal mycelial systems according to their patterns of différentiation and putative ecological importance. Mycorrhiza 11:107–114

    Article  Google Scholar 

  2. Alarcon-Gutierrez E, Floch C, Augur C, Le Petit J, Ziarelli F, Criquet S (2009) Spatial variations of chemical composition, microbial functional diversity, and enzyme activities in a Mediterranean litter (Quercus ilex L.) profile. Pedobiologia 52:387–399

    Article  CAS  Google Scholar 

  3. Ausec L, Zarkrzewski M, Goesmann A, Schlüter A, Mandic-Mulec I (2011) Bioinformatic analysis reveals high diversity of bacterial laccase-like enzymes. PLoS One 6:e25724

    Article  PubMed  CAS  Google Scholar 

  4. Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30:215–242

    Article  PubMed  CAS  Google Scholar 

  5. Baldrian P, Stursova M (2011) Enzymes in forest soils. Soil Biol Biochem 22:61–73

    Article  Google Scholar 

  6. Béguin P (1990) Mol Biol Cellul Degrad Annu Rev Microbiol 44:219–248

    Article  Google Scholar 

  7. Bell CW, Acosta-Martinez V, McIntyre NE, Cox S, Tissue DT, Zak JC (2009) Linking microbial community structure and function to seasonal differences in soil moisture and temperature in a Chihuahuan desert grassland. Microb Ecol 58:827–842

    Article  PubMed  CAS  Google Scholar 

  8. Biely P, Puls J, Schneider H (1985) Acetyl xylan esterases in fungal cellulolytic systems. FEBS Lett 186:80–84

    Article  CAS  Google Scholar 

  9. Brooks DD, Chan R, Starks ER, Grayston SJ, Jones MD (2011) Ectomycorrhizal hyphae structure components of the soil bacterial community for decreased phosphatase production. FEMS Microbiol Ecol 76:245–255

    Article  PubMed  CAS  Google Scholar 

  10. Buée M, Maurice JP, Zeller B, Andrianarisoa S, Ranger J, Courtecuisse R, Marçais B, Le Tacon F (2011) Influence of tree species on richness and diversity of epigeous fungal communities in a French temperate forest stand. Fungal Ecol 4:22–31

    Article  Google Scholar 

  11. Bugg TDH, Ahmad M, Hardiman EM, Singh R (2011) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22:394–400

    Article  PubMed  CAS  Google Scholar 

  12. Calvaruso C, Turpault MP, Leclerc E, Frey-Klett P (2007) Impact of ectomycorrhizosphere on the functional diversity of soil bacterial and fungal communities from a forest stand in relation to nutrient mobilization processes. Microb Ecol 54:567–577

    Article  PubMed  Google Scholar 

  13. Calvaruso C, Turpault M-P, Leclerc E, Ranger J, Garbaye J, Uroz S, Frey-Klett P (2010) Forest trees influence distribution of the mineral weathering bacterial communities from the Scleroderma citrinum mycorrhizosphere. Appl Environ Microbiol 76:4780–4787

    Article  PubMed  CAS  Google Scholar 

  14. Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J (2005) Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol 167:309–319

    Article  PubMed  CAS  Google Scholar 

  15. Courty PE, Pouysegur R, Buée M, Garbaye J (2006) Laccase and phosphatase activities of the dominant ectomycorrhizal types in a lowland oak forest. Soil Biol Biochem 38:1219–1222

    Article  CAS  Google Scholar 

  16. Courty PE, Hoegger PJ, Kilaru S, Kohler A, Buée M, Garbaye J, Martin F, Kües U (2009) Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycète Laccaria bicolor. New Phytol 182:736–750

    Article  PubMed  CAS  Google Scholar 

  17. Courty PE, Buée M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault MP, Uroz S, Garbaye J (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem 42:679–698

    Article  CAS  Google Scholar 

  18. Courty PE, Labbe J, Kohler A, Marçais B, Bastien C, Churin JL, Garbaye J, Le Tacon F (2011) Effect of poplar genotypes on mycorrhizal infection and secreted enzyme activities in mycorrhizal and non-mycorrhizal roots. J Exp Bot 62:249–260

    Article  PubMed  CAS  Google Scholar 

  19. Criquet S, Tagger S, Vogt G, Iacazio G, LePetit J (1999) Laccase activity of forest litter. Soil Biol Biochem 31:1239–1244

    Article  CAS  Google Scholar 

  20. de Boer W, Leveau JH, Kowalchuk GA, Klein Gunnewiek PJ, Abeln EC, Figge MJ, Sjollema K, Janse JD, van Veen JA (2004) Collimonas fungivorans gen. nov., sp. nov., a chitinolytic soil bacterium with the ability to grow on living fungal hyphae. Int J Syst Evol Microbiol 54:857–864

    Article  PubMed  Google Scholar 

  21. Frey-Klett P, Garbaye J, Tarkka M (2007) Tansley review: the mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  PubMed  CAS  Google Scholar 

  22. Gramms G, Günther T, Fritsche W (1998) Spot tests on oxidative enzymes in ectomycorrhizal, wood- and litter decaying fungi. Mycol Res 102:67–72

    Article  Google Scholar 

  23. Gügi B, Orange N, Hellio F, Burini JF, Guillou C, Leriche F, Guespin-Michel JF (1991) Effect of growth temperature on several exported enzyme activities in the psychrotropic bacterium Pseudomonas fluorescens. J Bacteriol 173:3814–3820

    PubMed  Google Scholar 

  24. Hoppe HG (1983) Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser 11:299–308

    Article  CAS  Google Scholar 

  25. Hsu SC, Lockwood JL (1975) Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 29:422–426

    PubMed  CAS  Google Scholar 

  26. Kellner H, Luis P, Zimdars B, Kiesel B, Buscot F (2008) Diversity of laccase-like multicopper oxidase genes in forest and grassland Cambisol soil samples. Soil Biol Biochem 40:638–648

    Article  CAS  Google Scholar 

  27. Kirk TK, Farrell RL (1987) Enzymatic “ combustion”: The microbial degradation of lignin. Annu Rev Microbiol 41:465–505

    Article  PubMed  CAS  Google Scholar 

  28. Koide RT, Sharda JN, Herr JR, Malcolm GM (2008) Ectomycorrhizal fungi and the biotrophy–saprotrophy continuum. New Phytol 178:230–233

    Article  PubMed  Google Scholar 

  29. Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant–microbe–soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115

    Article  CAS  Google Scholar 

  30. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–176

    Google Scholar 

  31. Lehman RM, O’Connell SP (2002) Comparison of extracellular enzyme activities and community composition of attached and free-living bacteria in porous medium columns. Appl Environ Microbiol 68:1569–1575

    Article  PubMed  CAS  Google Scholar 

  32. Leveau JHJ, Uroz S, de Boer W (2009) The bacterial genus Collimonas: mycophagy, weathering, and other adaptive solutions to life in oligotrophic environments. Environ Microbiol 12:281–292

    Article  PubMed  Google Scholar 

  33. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577

    Article  PubMed  CAS  Google Scholar 

  34. Niku-Paavola ML, Raaska L, Itävaara M (1990) Detection of white-rot fungi by a non-toxic stain. Mycol Res 94:27–31

    Article  Google Scholar 

  35. Peng X, Masai E, Kitayama H, Harada K, Katayama Y, Fukuda M (2002) Characterization of the 5-carboxyvanillate decarboxilase gene and its role in lignin related biphenyl catabolism in Sphingomonas paucimobilis SYK-6. Appl Environ Microbiol 68:4407–4415

    Article  PubMed  CAS  Google Scholar 

  36. Poole EJ, Bending GD, Whipps JM, Read DJ (2001) Bacteria associated with Pinus sylvestrisLactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro. New Phytol 151:553–766

    Article  Google Scholar 

  37. Pritsch K, Esperschuetz J, Haeler F, Raidl S, Winkler B, Schloter M (2009) Structure and activities of ectomycorrhizal and microbial communities in the rhizosphere of Fagus sylvatica under ozone and pathogen stress in a lysimeter study. Plant Soil 323:97–109

    Article  CAS  Google Scholar 

  38. Rambelli A (1973) The rhizosphere of mycorrhizae. In: Marks GC, Kozlowski TT (eds) Ectomycorrhizae, their ecology and physiology. Academic, New York, pp 299–349

    Google Scholar 

  39. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Article  PubMed  CAS  Google Scholar 

  40. Sinsabaugh RL (2005) Fungal enzymes at the community scale. In: Dighton J, Oudermans P, White J (eds) The fungal community, 3rd edn. CRC, New York, pp 237–247

    Google Scholar 

  41. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  42. Stursova M, Zifcakova L, Leigh B, Burgess R, Baldrian P (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol. doi:10.1111/j.1574-6941.2012.01343.x

  43. Sun YP, Unestam T, Lucas SD, Johanson KJ, Kenne L, Finlay RD (1999) Exudation–reabsorption in mycorrhizal fungi, the dynamic interface for interaction with soil and other microorganisms. Mycorrhiza 9:137–144

    Article  CAS  Google Scholar 

  44. Ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca

    Google Scholar 

  45. Thompson JD, Higgins DJ, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  46. Timonen S, Jorgensen KS, Haahtela K, Sen R (1998) Bacterial community structure at defined locations of Pinus sylvestrisSuillus bovinus and Pinus sylvestrisPaxillus involutus mycorrhizospheres in dry pine forest humus and nursery peat. Can J Microbiol 44:499–513

    CAS  Google Scholar 

  47. Uroz S, Calvaruso C, Turpault MP, Pierrat JC, Mustin C, Frey-Klett P (2007) Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil. Appl Environ Microbiol 73:3019–3027

    Article  PubMed  CAS  Google Scholar 

  48. Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387

    Article  PubMed  CAS  Google Scholar 

  49. Uroz S, Oger P, Lepleux C, Collignon C, Frey-Klett P, Turpault MP (2011) Bacterial weathering and its contribution to nutrient cycling in temperate forest ecosystems. Res Microbiol 162:820–831

    Article  PubMed  CAS  Google Scholar 

  50. Uroz S, Oger PM, Morin E, Frey-Klett P (2012) Distinct ectomycorrhizospheres share similar bacterial communities composition as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl Environ Microbiol 78:3020–3024

    Article  PubMed  CAS  Google Scholar 

  51. Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846

    Article  CAS  Google Scholar 

  52. Zifcakova L, Dobiasova P, Kolarova Z, Koukol O, Baldrian P (2011) Enzyme activities of fungi associated with Picea abies needles. Fungal Ecol 4:427–436

    Article  Google Scholar 

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Acknowledgments

This work was funded the Lorraine Region and INRA. Sequencing facilities were supported by IFR110, the Lorraine Region and INRA. The authors thank J. Ranger for helpful discussions and C. Delaruelle for technical assistance. We thank Dr. S. Antony-Babu for review of the English language. Pierre-Emmanuel Courty is an Ambizione fellow of the Swiss National Science Foundation (PZ00P3_136651). The authors thank also the anonymous referees for their helpful comments on the manuscript.

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Correspondence to S. Uroz.

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S. Uroz and P. E. Courty contributed equally to this work.

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Uroz, S., Courty, P.E., Pierrat, J.C. et al. Functional Profiling and Distribution of the Forest Soil Bacterial Communities Along the Soil Mycorrhizosphere Continuum. Microb Ecol 66, 404–415 (2013). https://doi.org/10.1007/s00248-013-0199-y

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