Skip to main content
Log in

Inhibition of Mushroom Formation and Induction of Glycerol Release—Ecological Strategies of Burkholderia terrae BS001 to Create a Hospitable Niche at the Fungus Lyophyllum sp. Strain Karsten

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

We investigated the ecological strategies exerted by the soil bacterium Burkholderia terrae BS001 at the hyphae of the soil saprotrophic fungus Lyophyllum sp. strain Karsten. Recently, this bacterium has been reported to form biofilms around, and to comigrate with, growing hyphae of Lyophyllum sp. strain Karsten. In addition, it was found to be able to utilize fungal metabolites. Here, we extend this work to shed some light on the interactions between the bacterial and fungal partner which allow ecological success for the former. In standing liquid microcosms inoculated with Lyophyllum sp. strain Karsten, we detected, upon prolonged incubation, the formation of a mycelial mat at the liquid–air interface. From this mat, primordia were formed after 4–6 weeks, which eventually resulted in mushrooms. However, upon addition of strain BS001 to the bulk liquid, mushroom formation from the fungal mat was clearly inhibited, as evidenced by (1) the formation of significantly lower numbers of primordia and (2) a delay of the onset of primordia formation. Moreover and importantly, the presence of strain BS001 caused the fungus to secrete large amounts of exudates at the mycelial mat, whereas such exudation was absent from control (uninoculated) or Escherichia coli K12- or Variovorax paradoxus BS64-inoculated microcosms. In the exudates, glycerol was the main carbonaceous component, and this compound could be easily utilized by strain BS001. Thus, in different experimental set-ups with the fungal partner, strain BS001 was shown to grow in the fungal exudates on the mat. The two fungal-interactive phenotypes were specific for B. terrae strain BS001, as the other bacteria used in our study, i.e. E. coli K12 and V. paradoxus BS64, did not exhibit any of these phenomena.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Nazir R, Warmink JA, Boersma FGH, van Elsas JD (2010) Mechanisms that promote bacterial fitness in fungal-affected soil microhabitats. FEMS Microbiol Ecol 71:169–185

    Article  PubMed  CAS  Google Scholar 

  2. Shaw RK, Berger CN, Feys B, Knutton S, Pallen MJ, Frankel G (2008) Enterohemorrhagic Escherichia coli exploits EspA filaments for attachment to salad leaves. Appl Environ Microbiol 74:2908–2914

    Article  PubMed  CAS  Google Scholar 

  3. Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–888

    Article  PubMed  CAS  Google Scholar 

  4. Partida-Martinez LP, Monajembashi S, Greulich KO, Hertweck C (2007) Endosymbiont-dependent host reproduction maintains bacterial–fungal mutualism. Curr Biol 17:773–777

    Article  PubMed  CAS  Google Scholar 

  5. Partida-Martinez LP, de Looss CF, Ishida K, Ishida M, Roth M, Buder K, Hertweck C (2007) Rhizonin, the first mycotoxin isolated from the zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl Environ Microbiol 73:793–797

    Article  PubMed  CAS  Google Scholar 

  6. Lackner G, Möbius N, Scherlach K, Partida-Martinez LP, Winkler R, Schmitt I, Hertweck C (2009) Global distribution and evolution of a toxinogenic BurkholderiaRhizopus symbiosis. Appl Environ Microbiol 75:2982–2986

    Article  PubMed  CAS  Google Scholar 

  7. Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger U, Wirthner P, Haas D, Defago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHA0: importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol Plant Microbe Interact 5:4–13

    Article  CAS  Google Scholar 

  8. Rezzonico F, Binder C, Défago G, Moënne-Loccoz Y (2005) The type III secretion system of biocontrol Pseudomonas fluorescens KD targets the phytopathogenic Chromista Pythium ultimum and promotes cucumber protection. Mol Plant Microbe Interact 18:991–1001

    Article  PubMed  CAS  Google Scholar 

  9. Artursson V (2005) Bacterial–fungal interactions highlighted using microbiomics: potential application for plant growth enhancement. Doctoral Thesis, Swedish University of Agricultural Sciences, Uppsala

  10. Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  PubMed  CAS  Google Scholar 

  11. Duponnois R, Colombet A, Hien V, Thioulouse J (2005) The mycorrhizal fungus Glomus intraradices and rock phosphate amendment influence plant growth and microbial activity in the rhizosphere of Acacia holosericea. Soil Biol Biochem 37:1460–1468

    Article  CAS  Google Scholar 

  12. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13

    Article  PubMed  CAS  Google Scholar 

  13. Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266

    Article  PubMed  Google Scholar 

  14. Bonfante, Lozano (2000) A Burkholderia strain living inside the arbuscular mycorrhizal fungus Gigaspora margarita possesses the vacB gene, which is involved in host cell colonization by bacteria. Mycol Res 39:137–144

    Google Scholar 

  15. Lackner G, Moebius N, Hertweck C (2011) Endofungal bacterium controls its host by an hrp type III secretion system. ISME J 5:252–261

    Article  PubMed  CAS  Google Scholar 

  16. Lackner G, Moebius N, Partida-Martinez LP, Boland S, Hertweck C (2011) Evolution of an endofungal lifestyle: deductions from the Burkholderia rhizoxinica genome. BMC Genom 12:210

    Article  CAS  Google Scholar 

  17. Nazir R (2012) The ecological success of Burkholderia terrae BS001 and related strains in the mycosphere. Doctoral thesis, University of Groningen, The Netherlands

  18. Warmink JA, van Elsas JD (2009) Migratory response of soil bacteria to Lyophyllum sp. strain Karsten in soil microcosms. Appl Environ Microbiol 75:2820–2830

    Article  PubMed  CAS  Google Scholar 

  19. Wick LY, Remer R, Würz B, Reichenbach J, Braun S, Schäfer F, Harms H (2007) Effect of fungal hyphae on the access of bacteria to phenanthrene in soil. Environ Sci Technol 41:500–505

    Article  PubMed  CAS  Google Scholar 

  20. Boer WD, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    Article  PubMed  Google Scholar 

  21. Warmink JA, van Elsas JD (2008) Selection of bacterial populations in the mycosphere of Laccaria proxima: is type III secretion involved? ISME J 2:887–900

    Article  PubMed  CAS  Google Scholar 

  22. Warmink JA, Nazir R, Corten B, van Elsas JD (2011) Hitchhikers on the fungal highway: the helper effect for bacterial migration via fungal hyphae. Soil Biol Biochem 43:760–765

    Article  CAS  Google Scholar 

  23. Boersma FGH, Otten R, Warmink JA, Nazir R, van Elsas JD (2010) Selection of Variovorax paradoxus-like bacteria in the mycosphere and the role of fungal-released compounds. Soil Biol Biochem 42:2137–2145

    Article  CAS  Google Scholar 

  24. Cusano AM, Burlinson P, Deveau A, Vion P, Uroz S, Preston GM, Frey-Klett P (2011) Pseudomonas fluorescens BBc6R8 type III secretion mutants no longer promote ectomycorrhizal symbiosis. Environ Microbiol Rep 3:203–210

    Article  CAS  Google Scholar 

  25. Chang S (2009) Training manual on mushroom cultivation technology. United Nations–Asian and Pacific Centre for Agricultural Engineering and Machinery (APCAEM) 1–65

Download references

Acknowledgements

We gratefully acknowledge the help of Marten Staal and Miaozhi Zhang for CO2 measurements and technical assistance in the laboratory, respectively. We thank the higher education commission of Pakistan for the financial support. Furthermore, the Soil Biotechnology Foundation is acknowledged for the financial support to RN.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jan Dirk van Elsas.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(PPTX 332 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nazir, R., Warmink, J.A., Voordes, D.C. et al. Inhibition of Mushroom Formation and Induction of Glycerol Release—Ecological Strategies of Burkholderia terrae BS001 to Create a Hospitable Niche at the Fungus Lyophyllum sp. Strain Karsten. Microb Ecol 65, 245–254 (2013). https://doi.org/10.1007/s00248-012-0100-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0100-4

Keywords

Navigation