Mycobiology

The Korean Society of Mycology (한국균학회)
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A Survey of Termitomyces (Lyophyllaceae, Agaricales), Including a New Species, from a Subtropical Forest in Xishuangbanna, China

  • Ye, Lei (Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences) ;
  • Karunarathna, Samantha C. (Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences) ;
  • Li, Huli (Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences) ;
  • Xu, Jianchu (Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences) ;
  • Hyde, Kevin D. (Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences) ;
  • Mortimer, Peter E. (Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences)
  • Received : 2019.06.10
  • Accepted : 2019.09.10
  • Published : 2019.12.01
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Abstract

A survey of mushrooms was conducted in Xishuangbanna, Yunnan Province, China, in the rainy season (May to October) of 2012, 2013, and 2014, during which 16 specimens of Termitomyces were collected. Preliminary macro- and micro-characteristics, together with ITS sequence data, showed that four of the specimens belonged to a new species (Termitomyces fragilis), while the other 12 belonged to T. aurantiacus, T. eurrhizus, T. globules, T. microcarpus, and T. bulborhizus. In this paper, T. fragilis is introduced as a species new to science based on morphological characterization and phylogenetic analyses. Macro- and micro- morphological descriptions, color photographs and line drawings of the new species, and a phylogenetic tree to show the placement of the new species are provided. T. fragilis is then compared with other closely related taxa in the genus Termitomyces.

Keywords

References

  1. Engel MS, Grimaldi DA, Krishna K. Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am Museum Novitates. 2009;3650:1-27.
  2. Heim R. Nouvelles etudes descriptives sur les agarics termitophiles d'Afrique tropicale. Archives du Museum Nationale d'Histoire Naturelle Paris serie. 1942;6:107-166.
  3. Batra LR, Batra SWT. Termite-fungus mutualism. In: Batra LR, editor. Insect fungus symbiosis. Nutrition, mutualism and commensalism. Proceedings of the Second International Mycological Congress; 1977 August 27-September 3; University of South Florida, Tampa, Florida. New York: Wiley. Bels, P. J. - Pataragetvit. 1979. p. 117-163.
  4. Chang ST, Quimio TH. Tropical Mushrooms: biological nature and cultivation methods. Hong Kong: Chinese University Press; 1982. p. 445-461.
  5. Dighton J, White JJF, White J, et al. The Fungal Community: Its Organization and Role in the Ecosystem. Boca Raton, FL: CRC Press; 1992. p. 295-310.
  6. Froslev TG, Aanen DK, Laessoe T, et al. Phylogenetic relationships of Termitomyces and related taxa. Mycol Res. 2003;107(11):1277-1286. https://doi.org/10.1017/S0953756203008670
  7. Oso BA. Mushrooms and the Yoruba people of Nigeria. Mycologia. 1975;67(2):311-319. https://doi.org/10.2307/3758423
  8. Parent G, Thoen D. Food value of edible mushrooms from Upper-Shaba region. Econ Bot. 1977;31(4):436-445. https://doi.org/10.1007/BF02912557
  9. Ogundana SK, Fagade OE. Nutritive value of some Nigerian edible mushrooms. Food Chem. 1982;8(4):263-268. https://doi.org/10.1016/0308-8146(82)90028-0
  10. Purkayastha RP, Chandra A. Manual of Indian Edible Mushroom. New Delhi: Today and Tomorrow's Printers and Publishers; 1985. p. 41-48.
  11. Jones EBG, Whalley AJS, Hywel-Jones NL. A fungus foray to Chiang Mai market in northern Thailand. Mycologist. 1994;8(2):87-90. https://doi.org/10.1016/s0269-915x(09)80139-0
  12. Sangvichien E, Taylor-Hawksworth PA. Termitomyces mushrooms: a tropical delicacy. Mycologist. 2001;15(1):31-33. https://doi.org/10.1016/S0269-915X(01)80058-6
  13. Wei TZ, Tang BH, Yao YJ. Revision of Termitomyces in China. Mycotaxon. 2009;108(1):257-285. https://doi.org/10.5248/108.257
  14. Mortimer PE, Karunarathna SC, Li QH, et al. Prized edible Asian mushrooms: ecology, conservation and sustainability. Fungal Divers. 2012;56(1):31-47. https://doi.org/10.1007/s13225-012-0196-3
  15. Devi MB, Singh SM, Singh NI. Nutrient analysis of indigenous Termitomyces eurrhizus (Berk.) Heim of Manipur, India. Int J Curr Microbiol App Sci. 2014;3:491-496.
  16. Heim R. Etudes descriptives et experimentales sur les agarics termitophiles d' Afrique tropicales Memoires de l'Academie (royale) des. Sci. 1941;64(74):25-29.
  17. Natarajan K. South Indian Agaricales I. Termitomyces. Kavaka. 1976;3:63-66.
  18. Pegler DN, Vanhaecke M. Termitomyces of southeast Asia. Kew Bull. 1994;49(4):717-736. https://doi.org/10.2307/4118066
  19. Kone N, Soro B, Vanie-Leabo LPL, et al. Diversity, phenology and distribution of Termitomyces species in Cote d'Ivoire. Mycology. 2018;9(4):307-315. https://doi.org/10.1080/21501203.2018.1500498
  20. Gomez LD. Una nueva especie neotropical de Termitomyces (Agaricales: Tennitomycetaceae). Revista de Biologia Tropical/Int J Tropical Biol Conserv. 1994;42:439-441.
  21. Moncalvo JM, Lutzoni FM, Rehner SA, et al. Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Syst Biol. 2000;49(2):278-305. https://doi.org/10.1080/10635159950173852
  22. Aanen DK, Eggleton P, Rouland-Lefevre C, et al. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci USA. 2002;99(23):14887-14892. https://doi.org/10.1073/pnas.222313099
  23. Rouland-Lefevre C, Diouf MN, Brauman A, et al. Phylogenetic relationships in Termitomyces based on the nucleotide sequence of ITS: a first approach to elucidate the evolutionary history of the symbiosis between fungus-growing termites and their fungi. Mol Phylogenet Evol. 2002;22(3):423-429. https://doi.org/10.1006/mpev.2001.1071
  24. Teng SC. Fungi of China (in Chinese). Beijing: Science Press; 1963. p. 808.
  25. Zang M. Notes on the classification and distribution of Termitomyces from Yunnan. Acta Botanica Yunnanica. 1981;3:367-374.
  26. Yang ZL, Shuai JG. Termitomyces in Xishuangbana of Yunnan, China. (in Chinese). Edib. Fung. 1990;12(6):2.
  27. Wang X, Liu P. Resources investigation and studies on the wild commercial fungi in Yunnan. Biodivers Sci. 2002;10:318-325. https://doi.org/10.3321/j.issn:1005-0094.2002.03.011
  28. Shi MX, Zhu LI, Yang KY, et al. Analysis on the nutritional components in different parts of Termitomyces albuminosus. Food Res Dev. 2012;33:182-183.
  29. Tang LP, Yang ZL. Advances in fungal resources of the Lancang River-Mekong River Basin. Resources Sci. 2014;36:282-295.
  30. Xi J. Valuation of ecosystem services in Xishuangbanna biodiversity conservation corridors initiative pilot site, China. Greater Mekong subregion core environment program. 2009. [cited 2019 Oct 22]. Available from: https://surumer.unihohenheim.de/fileadmin/einrichtungen/surumer/ADB_Valuation_of_Ecosystem_Services_in_Xishuangbanna_BCI_Site.pdf
  31. Lu YY, Ao ZH, Lu ZM, et al. Analgesic and antiinflammatory effects of the dry matter of culture broth of Termitomyces albuminosus and its extracts. J Ethnopharmacol. 2008;120(3):432-436. https://doi.org/10.1016/j.jep.2008.09.021
  32. Tai LM, Zhao CY, Guo X, et al. Prospects of exploitation and utilization on several kinds of high economic value of wild edible and medicinal fungi resource in Yunnan. Edible Fungi Cn. 2013;32:4-6.
  33. Ya X, Li MJ. Studies on the biological characteristics of Termitomyces albuminosus hypha. Adv Material Res. 2013;709:810-813. https://doi.org/10.4028/www.scientific.net/AMR.709.810
  34. Katoh H, Miura TK, Shinzato N, et al. Genetic variation of symbiotic fungi cultivated by the Macrotermitine termite Odontotermes formosanus, (Isoptera: Termitidae) in the Ryukyu archipelago. Mol Ecol. 2002;11(8):1565-1572. https://doi.org/10.1046/j.1365-294X.2002.01535.x
  35. Mueller UG, Gerardo N. Fungus-farming insects: multiple origins and diverse evolutionary histories. Proc Natl Acad Sci USA. 2002;99(24):15247-15249. https://doi.org/10.1073/pnas.242594799
  36. Darlington J, Benson RB, Cook CE, et al. Resolving relationships in some African fungusgrowing termites (Termitidae, Macrotermitinae) using molecular phylogeny, morphology, and field parameters. Insect Soc. 2008;55(3):256-265. https://doi.org/10.1007/s00040-008-1012-7
  37. Kudo T. Termite-microbe symbiotic system and its efficient degradation of lignocellulose. Biosci Biotechnol Biochem. 2009;73(12):2561-2567. https://doi.org/10.1271/bbb.90304
  38. Osiemo ZB, Marten A, Kaib M, et al. Open relationships in the castles of clay: high diversity and low host specificity of Termitomyces fungi associated with fungus-growing termites in Africa. Insect Soc. 2010;57(3):351-363. https://doi.org/10.1007/s00040-010-0092-3
  39. Kone NA, Dosso K, Konate S, et al. Environmental and biological determinants of Termitomyces species seasonal fructification in central and southern Cote d'Ivoire. Insect Soc. 2011;58(3):371-382. https://doi.org/10.1007/s00040-011-0154-1
  40. Sawhasan P, Worapong J, Vinijsanun T. Morphological and molecular studies of selected Termitomyces species collected from 8 districts of Kanchanaburi province, Thailand. Th J Agr Sci. 2011;44:183-196.
  41. Adhikari MK, Durrieu G. The genus Termitomyces (edible fungi) from Nepal. Np Agr Res J. 2012;12:71-76.
  42. Mossebo DC, Essouman EPF, Machouart MC, et al. Phylogenetic relationships, taxonomic revision and new taxa of Termitomyces (Lyophyllaceae, Basidiomycota) inferred from combined nLSU and mtSSU-rDNA sequences. Phytotaxa. 2017;321(1):71-102. https://doi.org/10.11646/phytotaxa.321.1.3
  43. Bergemann SE, Largent DL. The site specific variables that correlate with the distribution of the Pacific Golden Chanterelle, Cantharellus formosus. For Ecol Manage. 2000;130(1-3):99-107. https://doi.org/10.1016/S0378-1127(99)00177-2
  44. Chen J, Zhao R, Parra LA, et al. Agaricus section Brunneopicti: a phylogenetic reconstruction with descriptions of four new taxa. Phytotaxa. 2015;192(3):145-168. https://doi.org/10.11646/phytotaxa.192.3.2
  45. Kornerup A, Wanscher JH. Methuen handbook of colour. 2nd Ed. London: Methuen and Company; 1967.
  46. Jayasiri SC, Hyde KD, Ariyawansa HA, et al. The Faces of Fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Divers. 2015;74(1):3-18. https://doi.org/10.1007/s13225-015-0351-8
  47. Index Fungorum 2019. [cited 2019 May 1]. Available from: http://www.indexfungorum.org/names.
  48. Largent DL. How to identify Mushrooms to genus I: Macroscopical Features. Eureka, Calif: Mad River Press; 1977.
  49. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics In: Nis MA, Gelfand DH, Sninsky JJ et al., editors. PCR protocols: a guide to methods and applications. In: Academic Press, New York, USA; 1990. p. 315-322.
  50. Thompson JD, Gibson TJ, Plewniak F, et al. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25(24):4876-4882. https://doi.org/10.1093/nar/25.24.4876
  51. Swofford DL. Paup: Phylogenetic analysis using parsimony (and other methods) 4.0. B5. Sunderland, Massachusetts: Sinauer Associates; 2001.
  52. Alvarez-Buylla ER, Pelaz S, Liljegren SJ, et al. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci USA. 2000;97(10):5328-5333. https://doi.org/10.1073/pnas.97.10.5328
  53. Huelsenbeck JP, Ronquist F, Nielsen R, et al. Bayesian inference of phylogeny and its impact on evolutionary biology. Science. 2001;294(5550):2310-2314. https://doi.org/10.1126/science.1065889
  54. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. BMC Bioinf. 2001;17(8):754-755. https://doi.org/10.1093/bioinformatics/17.8.754
  55. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. BMC Bioinf. 2003;19(12):1572-1574. https://doi.org/10.1093/bioinformatics/btg180
  56. Page RD. Tree View: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996;12:357-358.
  57. Bi ZS, Zheng GY, Li TH, et al. Macrofungus Flora of the Mountainous District of North Guangdong. Guangzhou, China: Guangdong Science and Technology Press; 1990.
  58. Heim R. Les Termitomyces du Congo Belge recueillis par Medame M. Goossens-Fontana. Bull Jard Bot Etat. 1951;21(3/4):205-222. https://doi.org/10.2307/3666672
  59. He XS. Species and distribution of Termitomyces in China. Edib Fung. 1995;17:3-4.
  60. Wei TZ, Yao YJ, Wang B, et al. Termitomyces bulborhizus sp. nov. from China, with a key to allied species. Mycol Res. 2004;108(12):1458-1462. https://doi.org/10.1017/S0953756204001042
  61. Fu ZY. Research on the biology of Termitomyces in Yunnan. Yunnan Agricultural University, Kunming. 2007.
  62. Fu ZY, Li RC. Preliminary study on the relationship between the system of Termitmyces from Yunnan. J Fujian Agri Forestr Univ Nat Sci Ed. 2009;38:271-274.
  63. Zhang YJ. Molecular phylogeny and coevolution between Termitomyces and fungus-growing termites in Yunnan [dissertation]. Yunnan, China: Yunnan Agricultural University; 2012.
  64. Huang FS, Zhu SM, Zm P. Chinese Zoology, Insecta, Isoptera. Vol 17. Beijing: Science Press; 2000.
  65. Osmundson TW, Robert VA, Schoch CL, et al. Filling gaps in biodiversity knowledge for macrofungi: contributions and assessment of an herbarium collection DNA barcode sequencing project. PLoS One. 2013;8(4):e62419. https://doi.org/10.1371/journal.pone.0062419
  66. You YH, Yoon H, Kang SM, et al. Cadophora malorum Cs-8-1 as a new fungal strain producing gibberellins isolated from Calystegia soldanella. J Basic Microbiol. 2013;53(7):630-634. https://doi.org/10.1002/jobm.201200002
  67. Zhang W, Du F, Wang L, et al. Hydrolysis of oligosaccharides by a thermostable a-galactosidase from Termitomyces eurrhizus. Int J Mol Sci. 2015;16(12):29226-29235. https://doi.org/10.3390/ijms161226159

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