Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Pyrosequencing and Taxonomic Composition of the Fungal Community from Soil of Tricholoma matsutake in Gyeongju

  • Jeong, Minji (Department of Life Sciences and Biotechnology, Kyungpook National University) ;
  • Choi, Doo-Ho (Department of Life Sciences and Biotechnology, Kyungpook National University) ;
  • Cheon, Woo-Jae (Department of Forest Environment, Gyeongsangbuk-do Forest Environment Research Institute) ;
  • Kim, Jong-Guk (Department of Life Sciences and Biotechnology, Kyungpook National University)
  • Received : 2021.03.12
  • Accepted : 2021.03.24
  • Published : 2021.05.28
Download PDF
⟨ Previous Next ⟩

Abstract

Tricholoma matsutake is an ectomycorrhizal fungus that has a symbiotic relationship with the root of Pinus densiflora. Soil microbial communities greatly affect the growth of T. matsutake, however, few studies have examined the characteristics of these communities. In the present study, we analyzed soil fungal communities from Gyeongju and Yeongdeok using metagenomic pyrosequencing to investigate differences in fungal species diversity, richness, and taxonomic composition between the soil under T. matsutake fruiting bodies (Sample 2) and soil where the fairy ring of T. matsutake was no longer present (Sample 1). The same spot was investigated three times at intervals of four months to observe changes in the community. In the samples from Yeongdeok, the number of valid reads was lower than that at Gyeongju. The operational taxonomic units of most Sample 2 groups were less than those of Sample 1 groups, indicating that fungal diversity was low in the T. matsutake-dominant soil. The soil under the T. matsutake fruiting bodies was dominated by more than 51% T. matsutake. From fall to the following spring, the ratio of T. matsutake decreased. Basidiomycota was the dominant phylum in most samples. G-F1-2, G-F2-2, and Y-F1-2 had the genera Tricholoma, Umbelopsis, Oidiodendron, Sagenomella, Cladophialophora, and Phialocephala in common. G-F1-1, G-F2-1, and Y-F1-1 had 10 genera including Umbelopsis and Sagenomella in common. From fall to the following spring, the amount of phyla Basidiomycota and Mucoromycota gradually decreased but that of phylum Ascomycota increased. We suggest that the genus Umbelopsis is positively related to T. matsutake.

Keywords

Acknowledgement

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), Ministry of Education (2016R1A6A1A05011910), and the Research Institute for Dok-do and Ulleung-do Island of Kyungpook National University.

References

  1. Ahn JS, Lee KH. 1986. Studies on the volatile aroma components of edible mushroom (Tricholoma matsutake) of Korea. J. Kor. Soc. Food Nutr. 15: 253-257.
  2. Hoshi H, Yagi Y, Iijima H, Matsunaga K, Ishihara Y, Yasuhara T. 2005. Isolation and characterization of a novel immunomodulatory alpha-glucan-protein complex from the mycelium of Tricholoma matsutake in basidiomycetes. J. Agric. Food Chem. 53: 8948-8956. https://doi.org/10.1021/jf0510743
  3. Kim JY, Byeon SE, Lee YG, Lee JY, Park J, Hon, EK, et al. 2008. Immunostimulatory activities of polysaccharides from liquid culture of pine-mushroom Tricholoma matsutake. J. Microbiol. Biotechnol. 18: 95-103.
  4. Kim SY, Go KC, Song YS, Jeong YS, Kim EJ, Kim, BJ. 2014. Extract of the mycelium of T. matsutake inhibits elastase activity and TPA-induced MMP-1 expression in human fibroblasts. Int. J. Mol. Med. 34: 1613-1621. https://doi.org/10.3892/ijmm.2014.1969
  5. Hou Y, Ding X, Hou W, Zhong J, Zhu H, Ma B, et al. 2013. Anti-microorganism, anti-tumor, and immune activities of a novel polysaccharide isolated from Tricholoma matsutake. Pharmacogn Mag. 9: 244-249. https://doi.org/10.4103/0973-1296.113278
  6. Ohnuma N, Amemiya K, Kakuda R, Yaoita Y, Machida K, Kikuchi M. 2000. Sterol constituents from the edible mushrooms, Lentinula edodes and Tricholoma matsutake. Chem. Pharm. Bull. 48: 749-751. https://doi.org/10.1248/cpb.48.749
  7. Park C. 2020. 2019 Production of Forest Products. Korea Forest Service.
  8. Yamada A, Kanekawa S, Ohmasa M. 1999. Ectomycorrhiza formation of Tricholoma matsutake on Pinus densiflora. Mycoscience 40: 193-198. https://doi.org/10.1007/BF02464298
  9. Yamada A, Maeda K, Ohmasa M. 1999. Ectomycorrhiza formation of Tricholoma matsutake isolates on seedlings of Pinus densiflora in vitro. Mycoscience 40: 455-463. https://doi.org/10.1007/BF02461022
  10. Narimatsu M, Koiwa T, Masaki T, Sakamoto Y, Ohmori H. 2015. Relationship between climate, expansion rate, and fruiting in fairy rings ('shiro') of an ectomycorrhizal fungus Tricholoma matsutake in a Pinus densiflora forest. Fungal Ecol. 15: 18-28. https://doi.org/10.1016/j.funeco.2015.02.001
  11. Kataoka R, Siddiqui ZA, Kikuchi J, Ando M, Sriwati R, Nozaki A, et al. 2012. Detecting nonculturable bacteria in the active mycorrhizal zone of the pine mushroom Tricholoma matsutake. J. Microbiol. 50: 199-206. https://doi.org/10.1007/s12275-012-1371-7
  12. Kim M, Yoon H, You YH, Kim YE, Woo JR. 2013. Metagenomic analysis of fungal communities inhabiting the fairy ring zone of Tricholoma matsutake. J. Microbiol. Biotechnol. 23: 1347-1356. https://doi.org/10.4014/jmb1306.06068
  13. Lian C, Narimatsu M, Nara K, Hogetsu T. 2006. Tricholoma matsutake in a natural Pinus densiflora forest: correspondence between above- and below-ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytol. 171: 825-836. https://doi.org/10.1111/j.1469-8137.2006.01801.x
  14. 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. https://doi.org/10.1128/AEM.05839-11
  15. Corrales A, Arnold AE, Ferrer A, Turner BL, Dalling JW. 2016. Variation in ectomycorrhizal fungal communities associated with Oreomunnea mexicana (Juglandaceae) in a Neotropical montane forest. Mycorrhiza 26: 1-17. https://doi.org/10.1007/s00572-015-0641-8
  16. Kirk PM, Cannon PF, David JC, Stalpers JA. 2001. Ainsworth and Bisby's Dictionary of the Fungi, 9th Ed. CABI publishing, Wallingford. Uk.
  17. Peterson RL, Massicotte HB, Melville LH. 2004. Mycorrhizas: anatomy and cell biology, National Research Council Research Press, Ottawa. USA.
  18. Roy M, Schimann H, Braga-Neto R, Da Silva RAE, Duque J, Frame D, et al. 2016. Diversity and distribution of ectomycorrhizal fungi from Amazonian lowland white-sand forests in Brazil and French Guiana. Biotropica 48: 90-100. https://doi.org/10.1111/btp.12297
  19. Wang B, Qiu YL. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299-363. https://doi.org/10.1007/s00572-005-0033-6
  20. Agerer R. 2006. Fungal relationships and structural identity of their ectomycorrhizae. Mycol. Prog. 5: 67-107. https://doi.org/10.1007/s11557-006-0505-x
  21. Harley JL. 1989. The significance of mycorrhiza. Mycol. Res. 92: 129-139. https://doi.org/10.1016/S0953-7562(89)80001-2
  22. Lang C, Seven J, Polle A. 2011. Host preferences and differential contributions of deciduous tree species shape mycorrhizal species richness in a mixed central European forest. Mycorrhiza 21: 297-308. https://doi.org/10.1007/s00572-010-0338-y
  23. Sabella E, Nutricati E, Aprile A, Miceli A, Sorce C, Lorenzi R, et al. 2015. Arthrinium phaeospermum isolated from Tuber borchii ascomata: the first evidence for a "Mycorrhization Helper Fungus"? Mycol. Progress 14: 59. https://doi.org/10.1007/s11557-015-1083-6
  24. Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA. 2011. Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl. Environ. Microbiol. 77: 5934-5944. https://doi.org/10.1128/AEM.05255-11
  25. Oh SY, 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. https://doi.org/10.1371/journal.pone.0168573
  26. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D. 2003. Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84: 2042-2050. https://doi.org/10.1890/02-0433
  27. Hollister EB, Schadt CW, Palumbo AV, Ansley RJ, Boutton TW. 2010. Structural and functional diversity of soil bacterial and fungal communities following woody plant encroachment in the southern Great Plains. Soil Biol. Biochem. 42: 1816-1824. https://doi.org/10.1016/j.soilbio.2010.06.022
  28. Kernaghan G. 2005. Mycorrhizal diversity: Cause and effect? Pedobiologia 49: 511-520. https://doi.org/10.1016/j.pedobi.2005.05.007
  29. Peay KG, Baraloto C, Fine PV. 2013. Strong coupling of plant and fungal community structure across western Amazonian rainforests. ISME J. 7: 1852-1861. https://doi.org/10.1038/ismej.2013.66
  30. Wu YT, Wubet T, Trogisch S, Both S, Scholten T. 2013. Forest age and plant species composition determine the soil fungal community composition in a Chinese subtropical forest. PLoS One 8: e66829. https://doi.org/10.1371/journal.pone.0066829
  31. Baptista P, Reis F, Pereira E, Tavares RM, Santos PM, Richard F, et al. 2015. Soil DNA pyrosequencing and fruitbody surveys reveal contrasting diversity for various fungal ecological guilds in chestnut orchards. Environ. Microbiol. Rep. 7: 946-954. https://doi.org/10.1111/1758-2229.12336
  32. Handelsman J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68: 669-685. https://doi.org/10.1128/MMBR.68.4.669-685.2004
  33. Shokralla S, Spall JL, Gibson JF, Hajibabaei M. 2012. Next-generation sequencing technologies for environmental DNA research. Mol. Ecol. 21: 1794-1805. https://doi.org/10.1111/j.1365-294X.2012.05538.x
  34. Streit WR, Schmitz RA. 2004. Metagenomics--the key to the uncultured microbes. Curr. Opin. Microbiol. 7: 492-498. https://doi.org/10.1016/j.mib.2004.08.002
  35. Cannon PF, Kirk PM. 2007. Fungal Families of the World, Wallingford, UK: CABI.
  36. Panaro NJ, Yuen PK, Sakazume T, Fortina P, Kricka LJ. 2000. Evaluation of DNA fragment sizing and quantification by the agilent 2100 bioanalyzer. Clin. Chem. 46: 1851-1853. https://doi.org/10.1093/clinchem/46.11.1851
  37. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6: 1621-1624. https://doi.org/10.1038/ismej.2012.8
  38. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120. https://doi.org/10.1093/bioinformatics/btu170
  39. Li W, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659. https://doi.org/10.1093/bioinformatics/btl158
  40. Heck KL, Van Belle G, Simberloff D. 1975. Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology 56: 1459-1461. https://doi.org/10.2307/1934716
  41. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541. https://doi.org/10.1128/AEM.01541-09
  42. Prendergast-Miller MT, Baggs EM, Johnson D. 2011. Nitrous oxide production by the ectomycorrhizal fungi Paxillus involutus and Tylospora fibrillosa. FEMS Microbiol. Lett. 316: 31-35. https://doi.org/10.1111/j.1574-6968.2010.02187.x
  43. Niskanen T, Liimatainen K, Nuytinck J, Kirk P, Ibarguren IO, Garibay-Orijel R, et al. 2018. Identifying and naming the currently known diversity of the genus Hydnum, with an emphasis on European and North American taxa. Mycologia 110: 890-918. https://doi.org/10.1080/00275514.2018.1477004
  44. Ogawa M. 1976. Studies on the artificial reproduction of Tricholoma matsutake (S. Ito et Imai) Sing. III. Effects of growth promotion of natural products on the vegetative growth of T. matsutake. Trans Mycol. Soc. Jpn. 17: 492-498.
  45. You YH, Yoon HJ, Woo JR, Rim SO, Lee JH, Kong WS, et al. 2011. Diversity of endophytic fungi isolated from the rootlet of Pinus densiflora colonized by Tricholoma matsutake. Kor. J. Mycol. 39: 223-226. https://doi.org/10.4489/KJM.2010.39.3.223
  46. Oh SY, Kim M, Eimes JA, Lim YW. 2018. Effect of fruiting body bacteria on the growth of Tricholoma matsutake and its related molds. PLoS One 13: e0190948. https://doi.org/10.1371/journal.pone.0190948
  47. Osono T. 2006. Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Can. J. Microbiol. 52: 701-716. https://doi.org/10.1139/w06-023
  48. Summerbell RC. 2005. From Lamarckian fertilizers to fungal castles: recapturing the pre-1985 literature on endophytic and saprotrophic fungi associated with ectomycorrhizal root systems. Stud. Mycol. 53: 191-256. https://doi.org/10.3114/sim.53.1.191
  49. Tominaga Y. 1963. Studies on the life history of Japanese pine mushroom, Armillaria matsutake Ito et Imai. Bull. Hiroshima Agric. College 2: 105-145.
  50. Ogawa M. 1977. Microbial ecology of mycorrhizal fungus Tricholoma matsutake (S. Ito et Imai) Sing. in pine forest. III. Fungal florae in shiro soil and on the mycorrhiza. Bull. Government Forest Experimental Station 293: 105-170.
  51. Massee GE. 1914. Aspergillus cervinus Massee. Kew Misc. Bull. 4: 158.
  52. Elsohly HN, Slatkin DJ, Schiff Jr PL, Knapp JE. 1974. Metabolites of Aspergillus cervinus massee (Moniliaceae). J. Pharm. Sci. 63: 1632-1633. https://doi.org/10.1002/jps.2600631034
  53. Chen AJ, Varga J, Frisvad JC, Jiang XZ, Samson RA. 2016. Polyphasic taxonomy of Aspergillus section Cervini. Stud. Mycol. 85: 65-89. https://doi.org/10.1016/j.simyco.2016.11.001
  54. Park KH, Oh SY, Yoo S, Park MS, Fong JJ, Lim YW. 2020. Successional change of the fungal microbiome pine seedling roots inoculated with Tricholoma matsutake. Front. Microbial. 11: 2413.
  55. Cho DH, Lee KJ. 1995. A relationship between climatic factors and matsutake productions in 29 sites during a 10-year period in Korea. J. Korean Soc. For. Sci. 84: 277-285.
  56. Korea Meteorological Administration. 2015. Climate statistical analysis. Available from https://data.kma.go.kr/cmmn/main.do. Accessed Mar. 22, 2021.
  57. Chung DY, Lee KS, Lee JS, Youn YN. 2008. Characteristics of a forest soil on pine mushroom habitat located in Ponghwa, Kyungbuk and Gansung, Kangwon. 1. Physical and chemical properties of O horizon and surface soil. Kor. J. Soil Sci. Fert. 41: 206-213.
  58. 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. https://doi.org/10.1111/jam.12572
  59. Li Q, Li X, Chen C, Li S, Huang W, Xiong C, et al. 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. https://doi.org/10.4014/jmb.1505.05008