Microbial Ecology

, Volume 69, Issue 1, pp 146–159 | Cite as

Pairwise Transcriptomic Analysis of the Interactions Between the Ectomycorrhizal Fungus Laccaria bicolor S238N and Three Beneficial, Neutral and Antagonistic Soil Bacteria

  • Aurélie DeveauEmail author
  • Matthieu Barret
  • Abdala G. Diedhiou
  • Johan Leveau
  • Wietse de Boer
  • Francis Martin
  • Alain Sarniguet
  • Pascale Frey-Klett
Soil Microbiology


Ectomycorrhizal fungi are surrounded by bacterial communities with which they interact physically and metabolically during their life cycle. These bacteria can have positive or negative effects on the formation and the functioning of ectomycorrhizae. However, relatively little is known about the mechanisms by which ectomycorrhizal fungi and associated bacteria interact. To understand how ectomycorrhizal fungi perceive their biotic environment and the mechanisms supporting interactions between ectomycorrhizal fungi and soil bacteria, we analysed the pairwise transcriptomic responses of the ectomycorrhizal fungus Laccaria bicolor (Basidiomycota: Agaricales) when confronted with beneficial, neutral or detrimental soil bacteria. Comparative analyses of the three transcriptomes indicated that the fungus reacted differently to each bacterial strain. Similarly, each bacterial strain produced a specific and distinct response to the presence of the fungus. Despite these differences in responses observed at the gene level, we found common classes of genes linked to cell–cell interaction, stress response and metabolic processes to be involved in the interaction of the four microorganisms.


Hypothetical Protein Ectomycorrhizal Fungus Primary Metabolism Transcriptomic Response Saccharopine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



A. Deveau was supported by a scholarship from INRA, Lorraine Region and the Foreign Office exchange program Van Gogh. This work was supported by the French National Research Agency through the Laboratory of Excellence ARBRE (ANR-11-LABX-0002-01). We would like to thank A. Kohler for her help in submitting data to the GEO database and Aimee Orsini for proofreading the manuscript.


  1. 1.
    Bulgarelli D, Rott M, Schlaeppi K et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95PubMedCrossRefGoogle Scholar
  2. 2.
    Lundberg DS, Lebeis SL, Paredes SH et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. doi: 10.1038/nature11237 PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:260–270PubMedCentralPubMedGoogle Scholar
  4. 4.
    Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486PubMedCrossRefGoogle Scholar
  5. 5.
    Smith S, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Mycorrhizal symbiosis 800Google Scholar
  6. 6.
    Frey-Klett P, Burlinson P, Deveau A et al (2011) Bacterial–fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol Rev 75:583–609PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Horan DP, Chilvers GA (1990) Chemotropism: the key to ectomycorrhizal formation? New Phytol 116:297–301CrossRefGoogle Scholar
  8. 8.
    Deveau A, Palin B, Delaruelle C et al (2007) The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol 175:743–755PubMedCrossRefGoogle Scholar
  9. 9.
    Riedlinger J, Schrey SD, Tarkka MT et al (2006) Auxofuran, a novel metabolite that stimulates the growth of fly agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Appl Environ Microbiol 72:3550–3557. doi: 10.1128/AEM.72.5.3550-3557.2006 PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Aspray TJ, Jones EE, Davies MW et al (2013) Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp. Mycorrhiza 23:403–410PubMedCrossRefGoogle Scholar
  11. 11.
    Schrey SD, Schellhammer M, Ecke M et al (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216. doi: 10.1111/j.1469-8137.2005.01518.x PubMedCrossRefGoogle Scholar
  12. 12.
    Barret M, Frey-Klett P, Boutin M et al (2009) The plant pathogenic fungus Gaeumannomyces graminis var. tritici improves bacterial growth and triggers early gene regulations in the biocontrol strain Pseudomonas fluorescens Pf29Arp. New Phytol 181:435–447PubMedCrossRefGoogle Scholar
  13. 13.
    Chapon A, Guillerm A-Y, Delalande L et al (2002) Dominant colonisation of wheat roots by Pseudomonas fluorescens Pf29A and selection of the indigenous microflora in the presence of the take-all fungus. Eur J Plant Pathol 108:449–459CrossRefGoogle Scholar
  14. 14.
    Leveau JHJ, Uroz S, de Boer W (2010) The bacterial genus Collimonas: mycophagy, weathering and other adaptive solutions to life in oligotrophic soil environments. Environ Microbiol 12:281–292. doi: 10.1111/j.1462-2920.2009.02010.x PubMedCrossRefGoogle Scholar
  15. 15.
    Di Battista C, Selosse M-A, Bouchard D et al (1996) Variations in symbiotic efficiency, phenotypic charachters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S238. Mycol Res 100:1315–1324CrossRefGoogle Scholar
  16. 16.
    Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual. 1626Google Scholar
  17. 17.
    Baldi P, Long AD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17:509–519PubMedCrossRefGoogle Scholar
  18. 18.
    Duplessis S, Courty PE, Tagu D, Martin F (2005) Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol 165:599–611PubMedCrossRefGoogle Scholar
  19. 19.
    Mela F, Fritsche K, de Boer W et al (2011) Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger. ISME J 5:1494–1504. doi: 10.1038/ismej.2011.29 PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Barret M, Frey-Klett P, Guillerm-Erckelboudt AY et al (2009) Effect of wheat roots infected with the pathogenic fungus Gaeumannomyces graminis var. tritici on gene expression of the biocontrol bacterium Pseudomonas fluorescens Pf29Arp. Mol Plant Microbe Interact 22:1611–1623PubMedCrossRefGoogle Scholar
  21. 21.
    Frey P, Frey-Klett P, Garbaye J et al (1997) Metabolic and genotypic fingerprinting of fluorescent Pseudomonads associated with the Douglas fir—Laccaria bicolor mycorrhizosphere. Appl Environ Microbiol 63:1852–1860PubMedCentralPubMedGoogle Scholar
  22. 22.
    Uroz S, Courty PE, Pierrat JC et al (2013) Functional profiling and distribution of the forest soil bacterial communities along the soil mycorrhizosphere continuum. Microb Ecol 66:404–415. doi: 10.1007/s00248-013-0199-y PubMedCrossRefGoogle Scholar
  23. 23.
    Traxler MF, Watrous JD, Alexandrov T et al (2013) Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. mBio. doi: 10.1128/mBio.00459-13 PubMedCentralPubMedGoogle Scholar
  24. 24.
    Schroeckh V, Scherlach K, Nützmann H-W et al (2009) Intimate bacterial–fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 106:14558–14563. doi: 10.1073/pnas.0901870106 PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Gasch AP, Werner-Washburne M (2002) The genomics of yeast responses to environmental stress and starvation. Funct Integr Genom 2:181–192. doi: 10.1007/s10142-002-0058-2 CrossRefGoogle Scholar
  26. 26.
    Xie X, Wilkinson HH, Correa A et al (2004) Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa. Fungal Genet Biol 41:1104–1119. doi: 10.1016/j.fgb.2004.08.009 PubMedCrossRefGoogle Scholar
  27. 27.
    Paoletti M, Saupe SJ (2009) Fungal incompatibility: evolutionary origin in pathogen defense? Bioessays 31:1201–1210. doi: 10.1002/bies.200900085 PubMedCrossRefGoogle Scholar
  28. 28.
    Silar P (2012) Hyphal interference: self versus non self fungal recognition and hyphal death. In: Guenther W (ed) Biocommunication of fungi. Springer, New York, pp 155–170CrossRefGoogle Scholar
  29. 29.
    Huh CG, Aldrich J, Mottahedeh J et al (1998) Cloning and characterization of Physarum polycephalum tectonins. Homologues of Limulus lectin L-6. J Biol Chem 273:6565–6574PubMedCrossRefGoogle Scholar
  30. 30.
    Low DHP, Frecer V, Le Saux A et al (2010) Molecular interfaces of the galactose-binding protein tectonin domains in host–pathogen interaction. J Biol Chem 285:9898–9907. doi: 10.1074/jbc.M109.059774 PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Wohlschlager T, Butschi A, Grassi P et al (2014) Methylated glycans as conserved targets of animal and fungal innate defense. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1401176111
  32. 32.
    Peng X, Sun J, Iserentant D et al (2001) Flocculation and coflocculation of bacteria by yeasts. Appl Microbiol Biotechnol 55:777–781PubMedCrossRefGoogle Scholar
  33. 33.
    Marchi M, Boutin M, Gazengel K et al (2013) Genomic analysis of the biocontrol strain Pseudomonas fluorescens Pf29Arp with evidence of T3SS and T6SS gene expression on plant roots. Environ Microbiol Rep 5:393–403. doi: 10.1111/1758-2229.12048 PubMedCrossRefGoogle Scholar
  34. 34.
    Daval S, Lebreton L, Gazengel K et al (2011) The biocontrol bacterium Pseudomonas fluorescens Pf29Arp strain affects the pathogenesis-related gene expression of the take-all fungus Gaeumannomyces graminis var. tritici on wheat roots. Mol Plant Pathol 12:839–854PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Cumming J, Swiger T, Kurnik B, Panaccione D (2001) Organic acid exudation by Laccaria bicolor and Pisolithus tinctorius exposed to aluminum in vitro. Can J For Res 31:703–710Google Scholar
  36. 36.
    Ruijter GJG, van de Vondervoort PJI, Visser J (1999) Oxalic acid production by Aspergillus niger: an oxalate-non-producing mutant produces citric acid at pH 5 and in the presence of manganese. Microbiology 145:2569–2576PubMedGoogle Scholar
  37. 37.
    Sabotič J, Kos J (2012) Microbial and fungal protease inhibitors—current and potential applications. Appl Microbiol Biotechnol 93:1351–1375. doi: 10.1007/s00253-011-3834-x PubMedCrossRefGoogle Scholar
  38. 38.
    Sabotič J, Kilaru S, Budič M et al (2011) Protease inhibitors clitocypin and macrocypin are differentially expressed within basidiomycete fruiting bodies. Biochimie 93:1685–1693. doi: 10.1016/j.biochi.2011.05.034 PubMedCrossRefGoogle Scholar
  39. 39.
    Eissfeller V, Beyer F, Valtanen K et al (2013) Incorporation of plant carbon and microbial nitrogen into the rhizosphere food web of beech and ash. Soil Biol Biochem 62:76–81CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Aurélie Deveau
    • 1
    • 2
    • 8
    Email author
  • Matthieu Barret
    • 3
    • 6
  • Abdala G. Diedhiou
    • 1
    • 2
    • 7
  • Johan Leveau
    • 4
  • Wietse de Boer
    • 5
  • Francis Martin
    • 1
    • 2
  • Alain Sarniguet
    • 3
  • Pascale Frey-Klett
    • 1
    • 2
  1. 1.Interactions Arbres – MicroorganismesINRA UMR1136ChampenouxFrance
  2. 2.Interactions Arbres – MicroorganismesUniversité de Lorraine UMR1136Vandoeuvre-lès-NancyFrance
  3. 3.INRA UMR1349 IGEPPLe RheuFrance
  4. 4.Department of Plant PathologyUniversity of CaliforniaDavisUSA
  5. 5.Department of Microbial EcologyNetherlands Institute of Ecology (NIOO-KNAW)WageningenThe Netherlands
  6. 6.INRA – IRHSBeaucouzeFrance
  7. 7.Laboratoire Commun de MicrobiologieIRD/ISRA/UCAD Centre de Recherche de Bel-AirDakarSenegal
  8. 8.Interactions Arbres Micro-organismesINRA Lorraine Université, UMR 1136ChampenouxFrance

Personalised recommendations