Skip to main content
Log in

Effect of fairy ring bacteria on the growth of Tricholoma matsutake in vitro culture

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Tricholoma matsutake (pine mushroom) (Basidiomycota, Agaricales) is a valuable edible fungal species that cannot be cultivated artificially. As an ectomycorrhizal fungus, T. matsutake interacts with trees belonging to the Pinaceae and Fagaceae, and forms fairy rings around host trees that are arc-shaped areas with dense hyphae of T. matsutake in the soil. Because the fairy rings maintain their dense hyphae for several years and form fruiting bodies, the characteristics of the fairy ring may be important in understanding the ecology of T. matsutake. Recent studies have shown that diverse bacteria co-exist in the fairy ring, and suggest that the fairy ring bacteria may influence on the growth of T. matsutake. However, the effect of the fairy ring bacteria on the growth of T. matsutake is largely unknown. In this study, we isolated fairy ring bacteria and investigated their effect on the growth of T. matsutake in co-culture experiments. In addition, the relationship between bacterial effects and nutrient conditions was tested using different media with varying glucose concentrations. A total of 237 bacteria (28 species) were isolated from fairy rings of four different T. matsutake producing areas: Proteobacteria (17 species), Firmicutes (7 species), and Actinobacteria (4 species). Burkholderiaceae (Burkholderia and Paraburkholderia) was most abundant in the fairy ring bacteria communities. Most bacteria showed a negative effect on the growth of T. matsutake when it grew on glucose rich medium (20 g/L). In glucose deficient medium (2 g/L), however, some bacteria promoted the growth of T. matsutake. In addition, the mode of interaction between bacteria and T. matsutake is different, depending on the glucose concentration.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amann RI, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058

    Article  CAS  Google Scholar 

  • Brulé C, Frey-Klett P, Pierrat JC, Courrier S, Gérard F, Lemoine MC, Rousselet JL, Sommer G, 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 

  • Chen S, Qiu C, Huang T, Zhou W, Qi Y, Gao Y, Shen J, Qiu L (2013) Effect of 1-aminocyclopropane-1-carboxylic acid deaminase producing bacteria on the hyphal growth and primordium initiation of Agaricus bisporus. Fungal Ecol 6:110–118

    Article  Google Scholar 

  • Citterio B, Cardoni P, Potenza L, Amicucci A, Stocchi V, Gola G, Nuti M (1995) Isolation of bacteria from Sporocarps of Tuber Magnatum Pico, Tuber Borchii Vitt. and Tuber Maculatum Vitt. In: Stocchi V, Bonfante P, Nuti M (eds) Biotechnology of ectomycorrhizae. Springer, Berlin, pp 241–248

    Chapter  Google Scholar 

  • de Boer W, 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  Google Scholar 

  • Deveau A, Palin B, Delaruelle C, Peter M, Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, 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  CAS  Google Scholar 

  • Deveau A, Gross H, Palin B, Mehnaz S, Schnepf M, Leblond P, Dorrestein PC, Aigle B (2016) Role of secondary metabolites in the interaction between Pseudomonas fluorescens and soil microorganisms under iron-limited conditions. FEMS Microbiol Ecol 92: fiw107

    Article  Google Scholar 

  • Dobritsa AP, Samadpour M (2016) Transfer of eleven species of the genus Burkholderia to the genus Paraburkholderia and proposal of Caballeronia gen. nov. to accommodate twelve species of the genera Burkholderia and Paraburkholderia. Int J Syst Evol Microbiol 66:2836–2846

    Article  CAS  Google Scholar 

  • Duponnois R (1992) Les bactéries auxiliaires de la mycorhization du Douglas (Pseudotsuga menziesii (Mirb.) Franco) par Laccaria laccata souche S 238 (Doctoral dissertation)

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Garbaye J (1994) Tansley review no. 76 helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Article  Google Scholar 

  • Garbeva P, Hordijk C, Gerards S, de Boer W (2014) Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiol Ecol 87:639–649

    Article  CAS  Google Scholar 

  • Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 90:87–100

    Article  CAS  Google Scholar 

  • Huh TC, Joo SH, Park H, Chung JH (1998) Changes in soil physicochemical properties and dehydrogenase activity by the formation of fairy ring of Tricholoma matsutake. J Korean For Soc 87:270–275

    Google Scholar 

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

    Google Scholar 

  • Jolivet C, Angers DA, Chantigny MH, Andreux F, Arrouays D (2006) Carbohydrate dynamics in particle-size fractions of sandy spodosols following forest conversion to maize cropping. Soil Biol Biochem 38:2834–2842

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Kim MK, Math RK, Cho KM, Shin KJ, Kim JO, Ryu JS, Lee YH, Yun HD (2008) Effect of Pseudomonas sp. P7014 on the growth of edible mushroom Pleurotus eryngii in bottle culture for commercial production. Bioresour Technol 99:3306–3308

    Article  CAS  Google Scholar 

  • Kim M, Yoon H, Kim YE, Kim YJ, Kong WS, Kim JG (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  CAS  Google Scholar 

  • Labbe JL, Weston DJ, Dunkirk N, Pelletier DA, Tuskan GA (2014) Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus. Front Plant Sci 5:579

    PubMed  PubMed Central  Google Scholar 

  • Leveau JH, Preston GM (2008) Bacterial mycophagy: definition and diagnosis of a unique bacterial-fungal interaction. New Phytol 177:859–876

    Article  Google Scholar 

  • Li Q, Li X, Chen C, Li S, Huang W, Xiong C, Jin X, 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  CAS  Google Scholar 

  • Matsushita N, Kikuchi K, Sasaki Y, Guerin-Laguette A, Vaario LM, Suzuki K, Lapeyrie F, Intini M (2005) Genetic relationship of Tricholoma matsutake and T. nauseosum from the Northern Hemisphere based on analyses of ribosomal DNA spacer regions. Mycoscience 46:90–96

    Article  CAS  Google Scholar 

  • Nimaichand S, Tamrihao K, Yang LL, Zhu WY, Zhang YG, Li L, Tang S-K, Ningthoujam DS, Li WJ (2013) Streptomyces hundungensis sp. nov., a novel actinomycete with antifungal activity and plant growth promoting traits. J Antibiot 66:205–209

    Article  CAS  Google Scholar 

  • Ogawa M (1975) Microbial ecology of mycorrhizal fungus Tricholoma matsutake (Ito et Imai) Sing. in pine forest, I: fungal colony ('shiro') of Tricholoma matsutake. Bull Gov Exp Stat 272:79–121

    Google Scholar 

  • Oh S-Y, Fong JJ, Park MS, Lim YW (2016) Distinctive feature of microbial communities and bacterial functional profiles in Tricholoma matsutake dominant soil. PLoS One 11:e0168573

    Article  Google Scholar 

  • Ohara H, Hamada M (1967) Disappearance of bacteria from the zone of active mycorrhizas in Tricholoma matsutake (S. Ito et Imai) Singer. Nature 213:528–529

    Article  Google Scholar 

  • 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 151:743–751

    Article  Google Scholar 

  • Prenafeta-Boldu FX, Kuhn A, Luykx DM, Anke H, van Groenestijn JW, de Bont JA (2001) Isolation and characterisation of fungi growing on volatile aromatic hydrocarbons as their sole carbon and energy source. Mycol Res 105:477–484

    Article  CAS  Google Scholar 

  • Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-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 SD, Tarkka MT, Hampp R, Kapur M, Fiedler H-T (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  CAS  Google Scholar 

  • Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 5:429

    Article  Google Scholar 

  • Scherlach K, Graupner K, Hertweck C (2013) Molecular bacteria-fungi interactions: effects on environment, food, and medicine. Annu Rev Microbiol 67:375–397

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216

    Article  CAS  Google Scholar 

  • Stopnisek N, Zuhlke D, Carlier A, Barberan A, Fierer N, Becher D, Riedel K, Eberl L, Weisskopf L (2016) Molecular mechanisms underlying the close association between soil Burkholderia and fungi. ISME J 10:253–264

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tenorio-Salgado S, Tinoco R, Vazquez-Duhalt R, Caballero-Mellado J, Perez-Rueda E (2013) Identification of volatile compounds produced by the bacterium Burkholderia tropica that inhibit the growth of fungal pathogens. Bioengineered 4:236–243

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Varese G, Portinaro S, Trotta A, Scannerini S, Luppi-Mosca A, 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 

  • Wang Y, Hall IR, Evans LA (1997) Ectomycorrhizal fungi with edible fruiting bodies 1. Tricholoma matsutake and related fungi. Econ Bot 51:311–327

    Article  Google Scholar 

  • Warmink J, Nazir R, Van Elsas J (2009) Universal and species-specific bacterial ‘fungiphiles’ in the mycospheres of different basidiomycetous fungi. Environ Microbiol 11:300–312

    Article  CAS  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Yamaguchi M, Narimatsu M, Fujita T, Kawai M, Kobayashi H, Ohta A, Yamada A, Matsushita N, Neda H, Shimokawa T, Murata H (2016) A qPCR assay that specifically quantifies Tricholoma matsutake biomass in natural soil. Mycorrhiza 26:847–861

    Article  CAS  Google Scholar 

  • Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, 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  Google Scholar 

  • Young L-S, Chu J-N, Hameed A, Young C-C (2013) Cultivable mushroom growth-promoting bacteria and their impact on Agaricus blazei productivity. Pesqui Agropecu Bras 48:636–644

    Article  Google Scholar 

  • Zarei M, Aminzadeh S, Zolgharnein H, Safahieh A, Daliri M, Noghabi KA, Ghoroghi A, Motallebi A (2011) Characterization of a chitinase with antifungal activity from a native Serratia marcescens B4A. Braz J Microbiol 42:1017–1029

    Article  CAS  Google Scholar 

  • Zarenejad F, Yakhchali B, Rasooli I (2012) Evaluation of indigenous potent mushroom growth promoting bacteria (MGPB) on Agaricus bisporus production. World J Microbiol Biotechnol 28:99–104

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. Kang-Hyeon Ka and researcher Hee-Su Kim (Korea Forest Research Institute, South Korea) and Dr. Woo-Jae Chun (Gyeongbuk Forest Environment Research Institute, South Korea) for the assistance with sample collections, and Dr. Myung Soo Park (Seoul National University, South Korea) for the advice on experimental procedures. We would like to appreciate Dr. Rona Sturrock (Canadian Forest Service, Canada) for thoroughly reviewing the manuscript and the English editing. Isolate of T. matsutake was provided by Korea Mushroom Resource Bank (Seoul, South Korea).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Young Woon Lim.

Electronic supplementary material

Figure S1

The fairy ring of T. matsutake at sampling site. Grayish-white area in a red circle is the fairy ring of T. matsutake. Photograph was taken from a top-view after removing litter layers. (GIF 374 kb)

High Resolution Image (EPS 17442 kb)

Figure S2

Representative results of co-culture experiments in (a) a high glucose medium (hTMM) and (b) a low glucose medium (lTMM). Left: control plate without bacteria, center: Caballeronia sp., right: Paenibacillus taichungensis. (GIF 172 kb)

High Resolution Image (EPS 4.20 mb)

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. Effect of fairy ring bacteria on the growth of Tricholoma matsutake in vitro culture. Mycorrhiza 28, 411–419 (2018). https://doi.org/10.1007/s00572-018-0828-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-018-0828-x

Keywords

Navigation