Skip to main content
SpringerLink
Log in

Root-associated bacteria influencing mycelial growth of Tricholoma matsutake (pine mushroom)

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Tricholoma matsutake is an ectomycorrhizal fungus usually associated with Pinus densiflora in South Korea. Fruiting bodies (mushrooms) of T. matsutake are economically important due to their attractive aroma; yet, T. matsutake is uncultivatable and its habitat is rapidly being eradicated due to global climate change. Root-associated bacteria can influence the growth of ectomycorrhizal fungi that co-exist in the host rhizosphere and distinctive bacterial communities are associated with T. matsutake. In this study, we investigated how these bacterial communities affect T. matsutake growth by isolating bacteria from the roots of P. densiflora colonized by ectomycorrhizae of T. matsutake and co-culturing rootassociated bacteria with T. matsutake isolates. Thirteen species of bacteria (27 isolates) were found in pine roots, all belonging to the orders Bacillales or Burkholderiales. Two species in the genus Paenibacillus promoted the growth of T. matsutake in glucose poor conditions, likely using soluble metabolites. In contrast, other bacteria suppressed the growth of T. matsutake using both soluble and volatile metabolites. Antifungal activity was more frequent in glucose poor conditions. In general, pine rhizospheres harbored many bacteria that had a negative impact on T. matsutake growth and the few Paenibacillus species that promoted T. matsutake growth. Paenibacillus species, therefore, may represent a promising resource toward successful cultivation of T. matsutake.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams, A., Currie, C., Cardoza, Y., Klepzig, K., and Raffa, K. 2009. Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Can. J. For. Res. 39, 1133–1147.

    Article  CAS  Google Scholar 

  • Bal, A. and Chanway, C.P. 2012. Evidence of nitrogen fixation in lodgepole pine inoculated with diazotrophic Paenibacillus polymyxa. Botany 90, 891–896.

    Article  CAS  Google Scholar 

  • Behrendt, U., Schumann, P., Stieglmeier, M., Pukall, R., Augustin, J., Spröer, C., Schwendner, P., Moissl-Eichinger, C., and Ulrich, A. 2010. Characterization of heterotrophic nitrifying bacteria with respiratory ammonification and denitrification activity-Description of Paenibacillus uliginis sp. nov., an inhabitant of fen peat soil and Paenibacillus purispatii sp. nov., isolated from a spacecraft assembly clean room. Syst. Appl. Microbiol. 33, 328–336.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Benjamini, Y. and Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. 57, 289–300.

    Google Scholar 

  • Berge, O., Guinebretière, M.H., Achouak, W., Normand, P., and Heulin, T. 2002. Paenibacillus graminis sp. nov. and Paenibacillus odorifer sp. nov., isolated from plant roots, soil and food. Int. J. Syst. Evol. Microbiol. 52, 607–616.

    Article  PubMed  CAS  Google Scholar 

  • Brulé, C., Frey-Klett, P., Pierrat, J., Courrier, S., Gérard, F., Lemoine, M., Rousselet, J., Sommer, G., and Garbaye, J. 2001. Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and the effects of a mycorrhiza helper Pseudomonas fluorescens. Soil Biol. Biochem. 33, 1683–1694.

    Article  Google Scholar 

  • Calvaruso, C., Turpault, M.P., Leclerc, E., and 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 

  • Cusano, A.M., Burlinson, P., Deveau, A., Vion, P., Uroz, S., Preston, G.M., and Frey-Klett, P. 2011. Pseudomonas fluorescens BBc6R8 type III secretion mutants no longer promote ectomycorrhizal symbiosis. Environ. Microbiol. Rep. 3, 203–210.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Deveau, A., Palin, B., Delaruelle, C., Peter, M., Kohler, A., Pierrat, J.C., Sarniguet, A., Garbaye, J., Martin, F., and Frey-Klett, P. 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, 743–755.

    Article  PubMed  CAS  Google Scholar 

  • Dunstan, W., Malajczuk, N., and Dell, B. 1998. Effects of bacteria on mycorrhizal development and growth of container grown Eucalyptus diversicolor F. Muell. seedlings. Plant Soil 201, 241–249.

    Article  CAS  Google Scholar 

  • Duponnois, R. and Garbaye, J. 1990. Some mechanisms involved in growth stimulation of ectomycorrhizal fungi by bacteria. Can. J. Bot. 68, 2148–2152.

    Article  Google Scholar 

  • Duponnois, R. and Garbaye, J. 1991. Mycorrhization helper bacteria associated with the Douglas fir-Laccaria laccata symbiosis: effects in aseptic and in glasshouse conditions. Ann. For. Sci. 48, 239–251.

    Article  Google Scholar 

  • Ekblad, A. and Nordgren, A. 2002. Is growth of soil microorganisms in boreal forests limited by carbon or nitrogen availability? Plant Soil 242, 115–122.

    Article  CAS  Google Scholar 

  • Frey-Klett, P., Burlinson, P., Deveau, A., Barret, M., Tarkka, M., and Sarniguet, A. 2011. Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol. Mol. Biol. Rev. 75, 583–609.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Frey-Klett, P., Garbaye, J., and Tarkka, M. 2007. The mycorrhiza helper bacteria revisited. New Phytol. 176, 22–36.

    Article  PubMed  CAS  Google Scholar 

  • Garbaye, J. 1991. Biological interactions in the mycorrhizosphere. Cell. Mol. Life Sci. 47, 370–375.

    Article  Google Scholar 

  • Garbeva, P. and de Boer, W. 2009. Inter-specific interactions between carbon-limited soil bacteria affect behavior and gene expression. Microb. Ecol. 58, 36–46.

    Article  PubMed  CAS  Google Scholar 

  • Guerin-Laguette, A., Vaario, L.M., Matsushita, N., Shindo, K., Suzuki, K., and Lapeyrie, F. 2003. Growth stimulation of a Shirolike, mycorrhiza forming, mycelium of Tricholoma matsutake on solid substrates by non-ionic surfactants or vegetable oil. Mycol. Prog. 2, 37–43.

    Article  Google Scholar 

  • Guo, Y., Li, X., Zhao, Z., Wei, H., Gao, B., and Gu, W. 2017. Prediction of the potential geographic distribution of the ectomycorrhizal mushroom Tricholoma matsutake under multiple climate change scenarios. Sci. Rep. 7, 46221.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haas, D. and Défago, G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3, 307–319.

    Article  PubMed  CAS  Google Scholar 

  • Hampp, R. and Maier, A. 2008. Interaction between soil bacteria and ectomycorrhiza-forming fungi, pp. 197–210. In Varma, A., Abbott, L., Werner, D., and Hampp, R. (eds.), Plant surface microbiology. Springer, Berlin, Heidelberg, Germany.

    Chapter  Google Scholar 

  • Izumi, H., Anderson, I.C., Alexander, I.J., Killham, K., and Moore, E.R. 2006. Endobacteria in some ectomycorrhiza of Scots pine (Pinus sylvestris). FEMS Microbiol. Ecol. 56, 34–43.

    Article  PubMed  CAS  Google Scholar 

  • Izumi, H., Cairney, J.W., Killham, K., Moore, E., Alexander, I.J., and Anderson, I.C. 2008. Bacteria associated with ectomycorrhizas of slash pine (Pinus elliottii) in south-eastern Queensland, Australia. FEMS Microbiol. Lett. 282, 196–204.

    Article  PubMed  CAS  Google Scholar 

  • Izumi, H. and Finlay, R.D. 2011. Ectomycorrhizal roots select distinctive bacterial and ascomycete communities in Swedish subarctic forests. Environ. Microbiol. 13, 819–830.

    Article  PubMed  Google Scholar 

  • Izumi, H., Moore, E., Killham, K., Alexander, I., and Anderson, I. 2007. Characterisation of endobacterial communities in ectomycorrhizas by DNA- and RNA-based molecular methods. Soil Biol. Biochem. 39, 891–899.

    Article  CAS  Google Scholar 

  • Jeon, S.M. and Ka, K.H. 2015. Cultural characteristics of Korean ectomycorrhizal fungi. Korean J. Mycol. 43, 1–12.

    Article  Google Scholar 

  • Jiang, H., He, C., Yu, F., Liu, P., and Zhao, W. 2015. Bacterial diversity cultured from shiros of Tricholoma matsutake. Chin. J. Ecol. 34, 150–156.

    Google Scholar 

  • Ka, K.H., Kim, H.S., Jeon, S.M., Ryoo, R., Jang, Y., Wang, E.J., and Jeong, Y.S. 2017. Determination of the minimum size of seedlings with Matsutake mycelia that can survive in the field for Matsutake- infected pine tree production. Korean J. Mycol. 45, 188–195.

    Google Scholar 

  • Kai, M., Haustein, M., Molina, F., Petri, A., Scholz, B., and Piechulla, B. 2009. Bacterial volatiles and their action potential. Appl. Microbiol. Biotechnol. 81, 1001–1012.

    Article  PubMed  CAS  Google Scholar 

  • Kang, A., Cha, D., Kim, Y., Park, Y., and You, C. 1989. Studies on analyzing meteorological elements related with yield of Tricholoma matsutake (S. Ito et Imai) Singer. Korean J. Mycol. 17, 51–56.

    Google Scholar 

  • Kataoka, R., Siddiqui, Z.A., Kikuchi, J., Ando, M., Sriwati, R., Nozaki, A., and Futai, K. 2012. Detecting nonculturable bacteria in the active mycorrhizal zone of the pine mushroom Tricholoma matsutake. J. Microbiol. 50, 199–206.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Katoh, K. and Standley, D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim, I., Jung, G., Han, S., Cha, J., and Sung, J. 2005. Favorable condition for mycelial growth of Tricholoma matsutake. Korean J. Mycol. 33, 22–29.

    Article  Google Scholar 

  • Kim, Y.J. and Whang, K.S. 2007. Phylogenetic characteristics of viable but nonculturable bacterial populations in a pine mushroom (Tricholoma matsutake) forest soil. Korean J. Microbiol. 43, 201–209.

    Google Scholar 

  • Kim, M., Yoon, H., Kim, Y.E., Kim, Y.J., Kong, W.S., and Kim, J.G. 2014. Comparative analysis of bacterial diversity and communities inhabiting the fairy ring of Tricholoma matsutake by barcoded pyrosequencing. J. Appl. Microbiol. 117, 699–710.

    Article  PubMed  CAS  Google Scholar 

  • Labbé, J.L., Weston, D.J., Dunkirk, N., Pelletier, D.A., and Tuskan, G.A. 2014. Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus. Front. Plant. Sci. 5, 579.

    PubMed  PubMed Central  Google Scholar 

  • Li, Q., Li, X., Chen, C., Li, S., Huang, W., Xiong, C., Jin, X., and Zheng, L. 2016. Analysis of bacterial diversity and communities associated with Tricholoma matsutake fruiting bodies by barcoded pyrosequencing in Sichuan province, southwest China. J. Microbiol. Biotechnol. 26, 89–98.

    Article  PubMed  CAS  Google Scholar 

  • Linderman, R. 1988. Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78, 366–371.

    Google Scholar 

  • Marupakula, S., Mahmood, S., and Finlay, R.D. 2016. Analysis of single root tip microbiomes suggests that distinctive bacterial communities are selected by Pinus sylvestris roots colonized by different ectomycorrhizal fungi. Environ. Microbiol. 18, 1470–1483.

    Article  PubMed  CAS  Google Scholar 

  • Nazir, R., Warmink, J.A., Boersma, H., and Van Elsas, J.D. 2010. Mechanisms that promote bacterial fitness in fungal-affected soil microhabitats. FEMS Microbiol. Ecol. 71, 169–185.

    Article  PubMed  CAS  Google Scholar 

  • Oh, S.Y., Fong, J.J., Park, M.S., and Lim, Y.W. 2016. Distinctive feature of microbial communities and bacterial functional profiles in Tricholoma matsutake dominant soil. PLoS One 11, e0168573.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oh, S.Y., Kim, M., Eimes, J.A., and Lim, Y.W. 2018. Effect of fruiting body bacteria on the growth of Tricholoma matsutake and its related molds. PLoS One 13, e0190948.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Preston, G.M. 2007. Metropolitan microbes: type III secretion in multihost symbionts. Cell Host Microbe 2, 291–294.

    Article  PubMed  CAS  Google Scholar 

  • Raaijmakers, J.M., de Bruijn, I., and de Kock, M.J. 2006. Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol. Plant Microbe Interact. 19, 699–710.

    Article  PubMed  CAS  Google Scholar 

  • Raaijmakers, J.M., Paulitz, T.C., Steinberg, C., Alabouvette, C., and Moënne-Loccoz, Y. 2009. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321, 341–361.

    Article  CAS  Google Scholar 

  • Riedlinger, J., Schrey, S.D., Tarkka, M.T., Hampp, R., Kapur, M., and Fiedler, H.P. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmidt, R., Etalo, D.W., de Jager, V., Gerards, S., Zweers, H., de Boer, W., and Garbeva, P. 2016. Microbial small talk: Volatiles in fungal-bacterial interactions. Front. Microbiol. 6, 1495.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schrey, S.D., Schellhammer, M., Ecke, M., Hampp, R., and Tarkka, M.T. 2005. Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol. 168, 205–216.

    Article  PubMed  CAS  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Timonen, S. and Hurek, T. 2006. Characterization of culturable bacterial populations associating with Pinus sylvestris-Suillus bovinus mycorrhizospheres. Can. J. Microbiol. 52, 769–778.

    Article  PubMed  CAS  Google Scholar 

  • Tyc, O., Song, C., Dickschat, J.S., Vos, M., and Garbeva, P. 2017. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol. 25, 280–292.

    Article  PubMed  CAS  Google Scholar 

  • Vaario, L.M., Fritze, H., Spetz, P., Heinonsalo, J., Hanajik, P., and Pennanen, T. 2011. Tricholoma matsutake dominates diverse microbial communities in different forest soils. Appl. Environ. Microbiol. 77, 8523–8531.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Varese, G., Portinaro, S., Trotta, A., Scannerini, S., Luppi-Mosca, A., and Martinotti, M. 1996. Bacteria associated with Suillus grevillei sporocarps and ectomycorrhizae and their effects on in vitro growth of the mycobiont. Symbiosis 21, 129–147.

    Google Scholar 

  • Viollet, A., Corberand, T., Mougel, C., Robin, A., Lemanceau, P., and Mazurier, S. 2011. Fluorescent pseudomonads harboring type III secretion genes are enriched in the mycorrhizosphere of Medicago truncatula. FEMS Microbiol. Ecol. 75, 457–467.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Y., Hall, I.R., and Evans, L.A. 1997. Ectomycorrhizal fungi with edible fruiting bodies 1. Tricholoma matsutake and related fungi. Econ. Bot. 51, 311–327.

    Article  Google Scholar 

  • Warmink, J.A. and van Elsas, J.D. 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 

  • Weisburg, W.G., Barns, S.M., Pelletier, D.A., and Lane, D.J. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173, 697–703.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wheatley, R. 2002. The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie van Leeuwenhoek 81, 357–364.

    Article  PubMed  CAS  Google Scholar 

  • Yamada, A., Maeda, K., Kobayashi, H., and Murata, H. 2006. Ectomycorrhizal symbiosis in vitro between Tricholoma matsutake and Pinus densiflora seedlings that resembles naturally occurring ‘shiro’. Mycorrhiza 16, 111–116.

    Article  PubMed  Google Scholar 

  • Yamanaka, T., Ota, Y., Konno, M., Kawai, M., Ohta, A., Neda, H., Terashima, Y., and Yamada, A. 2014. The host ranges of coniferassociated Tricholoma matsutake, Fagaceae-associated T. bakamatsutake and T. fulvocastaneum are wider in vitro than in nature. Mycologia 106, 397–406.

    Article  PubMed  Google Scholar 

  • Yang, X., Luedeling, E., Chen, G., Hyde, K.D., Yang, Y., Zhou, D., Xu, J., and Yang, Y. 2012. Climate change effects fruiting of the prize matsutake mushroom in China. Fungal Divers. 56, 189–198.

    Article  Google Scholar 

  • Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., and Chun, J. 2017. Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole genome assemblies. Int. J. Syst. Evol. Microbiol. 67, 1613–1617.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zou, C.S., Mo, M.H., Gu, Y.Q., Zhou, J.P., and Zhang, K.Q. 2007. Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol. Biochem. 39, 2371–2379.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biological Sciences and Institute of Microbiology, Seoul National University, Seoul, 08826, Republic of Korea

    Seung-Yoon Oh & Young Woon Lim

Authors
  1. Seung-Yoon Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Young Woon Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Young Woon Lim.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oh, SY., Lim, Y.W. Root-associated bacteria influencing mycelial growth of Tricholoma matsutake (pine mushroom). J Microbiol. 56, 399–407 (2018). https://doi.org/10.1007/s12275-018-7491-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-018-7491-y

Keywords

Search

Navigation