Mycobiology

The Korean Society of Mycology (한국균학회)
권호 표지
DOI QR코드

DOI QR Code

New Species of Termitomyces (Lyophyllaceae, Basidiomycota) from Sabah (Northern Borneo), Malaysia

  • Seelan, Jaya Seelan Sathiya (Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah) ;
  • Yee, Chong Shu (Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah) ;
  • Fui, Foo She (Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah) ;
  • Dawood, Mahadimenakbar (Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah) ;
  • Tan, Yee Shin (Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah) ;
  • Kim, Min-Ji (Wood Utilization Division, Forest Products Department, National Institute of Forest Science) ;
  • Park, Myung Soo (School of Biological Sciences and Institute of Microbiology, Seoul National University) ;
  • Lim, Young Woon (School of Biological Sciences and Institute of Microbiology, Seoul National University)
  • Received : 2019.08.13
  • Accepted : 2020.02.13
  • Published : 2020.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

The genus Termitomyces (Lyophyllaceae, Basidiomycota) is often associated with fungus-feeding termites (Macrotermitinae) due to their strong symbiotic relationships. The genus is widely found exclusively in certain regions of Africa and Asia. They are recognized as edible mushroom within Southeast Asia as well. But it is often misidentified based on morphology by the local communities especially in Malaysia for Chlorophyllum molybdites which is a highly poisonous mushroom. Thus, it is necessary to study the genus for Malaysia with the synergy of using both morphological and molecular identification. In this study, we aim to describe another new species as an addition to the genus Termitomyces found within Sabah, Malaysia. We generated two new sequences (nrLSU and mtSSU) for the new species and a total of 28 nrLSU and mtSSU sequences were retrieved from GenBank for the phylogenetic analysis using maximum likelihood and Bayesian inferences. We identified that the new collection from Sabah province is a new species and named as Termitomyces gilvus based on the termites found in the mound. A phylogeny tree made from the concatenated genes of LSU and mtSSU suggests that T. gilvus is closely related to T. bulborhizus from China. According to our results, the combination of molecular and morphology proved to be a robust approach to re-evaluate the taxonomic status of Termitomyces species in Malaysia. Additional surveys are needed to verify the species diversity and clarify their geographic distribution.

Keywords

References

  1. 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
  2. Aanen DK, Eggleton P. Fungus-growing termites originated in African rain forest. Curr Biol. 2005;15(9):851-855. https://doi.org/10.1016/j.cub.2005.03.043
  3. Aanen DK. As you reap, so shall you sow: coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi. Biol Lett. 2006;2(2):209-212. https://doi.org/10.1098/rsbl.2005.0424
  4. Hyodo F, Tayasu I, Inoue T, et al. Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Funct Ecol. 2003;17(2):186-193. https://doi.org/10.1046/j.1365-2435.2003.00718.x
  5. Batra LR, Batra S. The fungus gardens of insects. Sci Am. 1967;217(5):112-120. https://doi.org/10.1038/scientificamerican1167-112
  6. Batra LR, Batra S. Termite-fungus mutualism. In: Batra LR, editor. Insect-fungus symbiosis. Nutrition, mutualism and commensalism. New York: Allanheld, Osmun and Co; 1979. p. 117-163.
  7. Kirk PM, Cannon PF, Minter DW, et al. Dictionary of the fungi. 10th ed. Wallingford, UK: CABI; 2008. p. 771.
  8. Mossebo DC, Essouman EPF, Machouart MC, et al. Phylogenetic relationships, taxonomic revision and new taxa of Termitomyces (Lyophyllaceae, Basidiomycota) inferred from combined nLSUand mtSSU-rDNA sequences. Phytotaxa. 2017;321(1):71-102. https://doi.org/10.11646/phytotaxa.321.1.3
  9. Pegler DN, Vanhaecke M. Termitomyces of Southeast Asia. Kew Bull. 1994;49(4):717-736. https://doi.org/10.2307/4118066
  10. Turnbull E, Watling R. Some records of Termitomyces from old world rainforests. Kew Bull. 1999;54(3):731-738. https://doi.org/10.2307/4110869
  11. 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
  12. Venkatachalapathi A, Paulsamy S. Exploration of wild medicinal mushroom species in Walayar valley, the Southern Western Ghats of Coimbatore District Tamil Nadu. Mycosphere. 2016;7(2):118-130. https://doi.org/10.5943/mycosphere/7/2/3
  13. Teke NA, Kinge TR, Bechem E, et al. Ethnomycological study in the Kilum-Ijim mountain forest, Northwest Region, Cameroon. J Ethnobiol Ethnomed. 2018;14(1):25 https://doi.org/10.1186/s13002-018-0225-8
  14. Hsieh HM, Ju YM. Medicinal components in Termitomyces mushrooms. Appl Microbiol Biotechnol. 2018;102(12):4987-4994. https://doi.org/10.1007/s00253-018-8991-8
  15. Froslev TG, Aanen DK, Rosendahl S, et al. Phylogenetic relationship of Termitomyces and related taxa. Mycol Res. 2003;107(11):1277-1286. https://doi.org/10.1017/S0953756203008670
  16. Chang ST, Quimio TH. Tropical mushrooms biological nature and cultivation methods. Hong Kong: The Chinese University Press; 1982. p. 493.
  17. Rouland-Lefevre C, Diouf MN, Brauman A, et al. Phylogenetic relationships in Termitomyces (family Agaricaceae) 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 Phylogenetics Evol. 2002;22(3):423-429. https://doi.org/10.1006/mpev.2001.1071
  18. Taprab Y, Ohkuma M, Johjima T, et al. Molecular phylogeny of symbiotic Basidiomycetes of fungus-growing termites in Thailand and their relationship with the host. Biosci Biotechnol Biochem. 2002;66(5):1159-1163. https://doi.org/10.1271/bbb.66.1159
  19. Sawhassan P, Worapong J, Vinijsanun T. Morphological and molecular studies of selected Termitomyces species collected from 8 districts of Kanchanaburi province, Thailand. Thai J Agric Sci. 2011;44:183-196.
  20. Chang YS, Lee SS. Utilisation of macrofungi in Malaysia. Fungal Divers. 2004;15:15-22.
  21. Azliza MA, Ong HC, Vikineswary S, et al. Ethnomedicinal resources used by the Temuan in Ulu Kuang Village. Stud Ethno-Med. 2012;6(1):17-22. https://doi.org/10.1080/09735070.2012.11886415
  22. Azliza MA. A comparison of ethnobiological knowledge between the Mah Meri and Temuan tribes in Selangor [master's thesis]. Kuala Lumpur: University of Malaya; 2013.
  23. Faridah A, Kanapathipillay V, Whalley M, et al. Termitomyces mushrooms: a tropical delicacy. Mycologist. 2002;16:9. https://doi.org/10.1016/S0269-915X(07)60014-7
  24. Abdullah F, Rusea G. Documentation of inherited knowledge on wild edible fungi from Malaysia. Blumea - J Plant Tax Plant Geog. 2009;54(1):35-38. https://doi.org/10.3767/000651909X475996
  25. Foo FS, Saikim FH, Kulip J, et al. Distribution and ethnomycological knowledge of wild edible mushrooms in Sabah (Northern Borneo, Malaysia. J Trop Biol Conserv. 2018;15:203-222.
  26. Siddiquee S, Rovina K, Naher L, et al. Phylogenetic relationships of Termitomyces aurantiacus inferred from internal transcribed spacers DNA sequences. Adv Biosci Biotechnol. 2015;06(05):358-367. https://doi.org/10.4236/abb.2015.65035
  27. Corner E. The seasonal fruiting of Agarics in Malaya. Gardens Bull Straits Settlement. 1935;9:79-88.
  28. Corner EJH. A discussion of the results of the Royal Society Expedition to North Borneo organized by E.J.H. Corner. J Proc Linn Soc Bot Series B. 1964;161:3-6 and 90-91.
  29. Corner E. 1981. The agaric genera Lentinus, Panus, and Pleurotus with particular reference to Malaysian species. Beih Nova Hedwigia. 1981;69:1-169.
  30. Corner EJH. I am part of all that I have met (Tennyson's Ulysses). In: Isaac S, Frankland JC, Watling R, Whalley AJS, editors. Aspects of tropical mycology. Cambridge: Cambridge University Press; 1993. p. 1-13.
  31. Corner E. Agarics in Malesia I. Tricholomatoid. II. Mycenoid. Beih Nova Hedwigia. 1994;109:1-271.
  32. Corner E. The Agaric Genera Marasmius, Chaetocalathus, Crinipellis, Heimiomyces, Resupinatus, Xerula and Xerulina in Malesia. Beih Nova Hedwigia. 1996;111:1-175.
  33. Hjortstam K, Spooner BM, Oldridge SG. Some Aphyllophorales and Heterobasidiomycetes from Sabah, Malaysia. Kew Bull. 1990;45(2):303-322. https://doi.org/10.2307/4115688
  34. Pegler DN. The larger fungi of Borneo. Kota Kinabalu: Natural History Publications; 1997. p. 95.
  35. Kornerup A, Wanscher JH. Methuen handbook of colour. 3rd ed. London: Eyre Methuen; 1978. p. 252.
  36. Ahmad M. Termites (Isoptera) of Thailand. B Am Mus Nat Hist. 1965;131:1-111.
  37. Eggleton P, Homathevi R, Jeeva D, et al. The species richness and composition of termites (Isoptera) in primary and regenerating lowland dipterocarp forest in Sabah, East Malaysia. Ecotropica. 1997;3:119-128.
  38. Largent DL, Johnson D, Watling R. How to identify mushrooms to genus, III. Microscopic features. Eureka: Mad River Press; 1977. p. 25-26.
  39. Bruns TD, Fogel R, Taylor JW. Amplification and sequencing of DNA from fungal herbarium specimens. Mycologia. 1990;82(2):175-184. https://doi.org/10.1080/00275514.1990.12025863
  40. White TJ, Bruns T, Lee S, et al. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols: a guide to methods and applications. New York: Academic Press; 1990. p. 315-322.
  41. Tamura K, Peterson D, Peterson N, et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28(10):2731-2739. https://doi.org/10.1093/molbev/msr121
  42. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772-780. https://doi.org/10.1093/molbev/mst010
  43. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES science gateway for inference of large phylogenetic trees. SC10 workshop on gateway computing environments (GCE10); 2010 Nov 13-19; New Orleans (LA): IEEE Computer Society; 2010. p. 1-8.
  44. Ronquist F, Teslenko M, Van Der Mark P, et al. MrBAYES 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539-542. https://doi.org/10.1093/sysbio/sys029
  45. Wei TZ, Tang BH, Yao YJ. Revision of Termitomyces in China. Mycotaxon. 2009;108(1):257-285. https://doi.org/10.5248/108.257
  46. Wei T, Yao Y, 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
  47. Kosakul TA, Boasri A, Chalermpongse, Kuhiran M. Genetic diversity of Termitomyces in central Thailand using isozyme markers. J Sci Res Chula Univ. 2007;32:63-72.

Cited by

  1. Isolation, identification, cultivation and determination of antimicrobial β-glucan from a wild-termite mushroom Termitomyces heimii RFES 230662 vol.37, 2020, https://doi.org/10.1016/j.bcab.2021.102187