Phylogenetic Relationships of Termitomyces aurantiacus Inferred from Internal Transcribed Spacers DNA Sequences


Fungus-growing termites cultivate species of the mutualistic basidiomycete genus Termitomyces on a substrate called the fungal comb. Identification of fungal species based on morphological features is complicated, tedious, and prone to errors. As an alternative, nuclear ribosomal DNA sequences consisting of the internal transcribed spacers (ITS1 and ITS2) and 5.8S rDNA were used to identify Malaysian isolates of Termitomyces sp. The morphological characteristics and molecular data indicate that Malaysian Termitomyces isolated is clearly monophyletic and belongs to the Tricholomataceae family. The Malaysian isolates analyzed in this study represent the termite fungus species called T. aurantiacus.

Share and Cite:

Siddiquee, S. , Rovina, K. , Naher, L. , Rodrigues, K. and Uzzaman, M. (2015) Phylogenetic Relationships of Termitomyces aurantiacus Inferred from Internal Transcribed Spacers DNA Sequences. Advances in Bioscience and Biotechnology, 6, 358-367. doi: 10.4236/abb.2015.65035.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Abe, T. and Matsumoto, T. (1979) Studies on the Distribution and Ecological Role of Termites in a Lowland Rainforest of West Malaysia. 3. Distribution and Abundance of Termites in Pasoh Forest Reserve. Japanese Journal of Ecology, 29, 337-351.
[2] Wood, T.G. and Sands, W.A. (1978) The Role of Termites in Ecosystems. In: Brain, M.V., Ed., Production Ecology of Ants and Termites. Cambridge, Cambridge University Press, 245-292.
[3] Schuurman, G. (2005) Decomposition Rates and Termite Assemblage Composition in Semiarid Africa. Ecology, 86, 1236-1249.
[4] Grassé, P.P. (1959) Une nouveau type de symbiose: La meule alimentaire des termites champignonnistes. Nature, 3293, 385-389.
[5] Kambhampati, S. and Eggleton, P. (2000) Taxonomy and Phylogenetics of Isoptera. In: Abe, T., Bignell, D.A. and Higashi, M., Eds., Termites: Evolution, Sociality, Symbioses and Ecology, Kluwer Academic Publishers, Dordrecht, 1-23.
[6] Kirk, P.M., Cannon, P.F., Minter, D.W., et al. (2008) Ainsworth & Bisbys Dictionary of the Fungi. 10th Edition, CABI Publishing, Wallingford, 771.
[7] Pegler, D.N. and Vanhaecke, M. (1994) Termitomyces of Southeast Asia. Kew Bulletin, 49, 717-736.
[8] Heim, R. (1977) Termites et Champignons. Les champignons termitophiles d’Afrique Noire et d’Asie me’ridionale. E’ ditions Boube’e, Paris, 205 p.
[9] Aanen, D.K., Eggleton, P., Rouland-Lefevre, C., et al. (2002) The Evolution of Fungus-Growing Termites and Their Mutualistic Fungal Symbionts. Proceedings of the National Academy of Sciences of the United States of America, 99, 14887-14892.
[10] Froslev, T.G., Aanen, D.K., Laessoe, T. and Rosendahl, S. (2003) Phylogenetic Relationships of Termitomyces and Related Taxa. Mycological Research, 107, 1277-1286.
[11] Rouland-Lefevre, C. (2000) Symbiosis with Fungi. In: Abe, T., Bignell, D.E. and Higashi, M., Eds., Termites: Evolution, Sociality, Symbioses, Ecology, Kluwer Academic Publishers, Dordrecht, 289-306.
[12] Edel, V. (1998) Use of PCR and RFLP in Fungal Systematic. In: Frisvad, J.C., Bridge, P.D. and Arora, D.K., Eds., Chemical Fungal Taxonomy, Marcel Dekka Inc., New York, 51-76.
[13] Taylor, J.W., Jacobson, D.J., Kroken, S., Kasuga, T., Geiser, D.M., Hibbett, D.S. and Fisher, M.C. (2000) Phylogenetic Species Recognition and Species Concepts in Fungi. Fungal Genetics and Biology, 31, 21-32.
[14] Reynolds, J., Weir, B.S. and Cockerham, C.C. (1983) Estimation of the Coancestry Coefficient: Basis for a Short-Term Genetic Distance. Genetics, 105, 767-779.
[15] Johnson, R.A., Thomas, R.J., Wood, T.G. and Swift, M.J. (1981) The Inoculation of the Fungus Comb in Newly Founded Colonies of Some Species of the Macrotermitinae (Isoptera) from Nigeria. Journal of Natural History, 15, 751-756.
[16] De Fine Licht, H.H., Boomsma, J.J. and Aanen, D.K. (2006) Presumptive Horizontal Symbiont Transmission in the Fungus-Growing Termite Macrotermes natalensis. Molecular Ecology, 15, 3131-3138.
[17] Nobre, T., Fernandes, C., Boomsma, J.J., Korb, J. and Aanen, D.K. (2011) Farming Termites Determine the Genetic Population Structure of Termitomyces Fungal Symbionts. Molecular Ecology, 20, 2023-2033.
[18] Hagn, A., Wallisch, S., Rad, V., Munch, J.C. and Schloter, M. (2007) A New Cultivation Independent Approach to Detect and Monitor Common Trichoderma Species in Soils. Journal of Microbiological Methods, 69, 86-92.
[19] Jansen, G., Devaere, S., Weekers, P.H.H. and Adriaens, D. (2006) Phylogenetic Relationships and Divergence Time Estimate of African Angulliform Catfish (Siluriformes: Clariidae) Inferred from Ribosomal Gene and Spacer Sequences. Molecular Phylogenetics and Evolution, 38, 65-78.
[20] Schocha, C.L., Seifertb, K.A., Huhndorf, S., Robertd, V., Spougea, J.L., André Levesqueb, C., et al. (2012) Fungal Barcoding Consortiuma, Nuclear Ribosomal Internal Transcribed Spacer (ITS) Region as a Universal DNA Barcode Marker for Fungi. PNAS, 109, 6241-6246.
[21] Young, I. and Coleman, A.W. (2004) The Advantages of the ITS2 Region of the Nuclear rDNA Cistron for Analysis of Phylogenetic Relationships of Insects: A Drosophila Example. Molecular Phylogenetics and Evolution, 30, 236-242.
[22] White, T.J., Bruns, T., Lee, S. and Taylor, J.W. (1990) Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. and White, T., Eds., PCR Protocols, Academic Press, San Diego, 315-322.
[23] Siddiquee, S., Yee, W.Y., Taslima, K., Fatihah, N.H.N., Kumar, S.V. and Hasan, M.M. (2012) Sequence Analysis of the Ribosomal DNA Internal Transcribed Spacer Regions in Termitomyces heimii Species. Annals of Microbiology, 62, 797-803.
[24] Thompson, J., Higgins, D. and Gibson, T. (1994) Clustal W: Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting Position-Specific Gap Penalties and Weight Matrix Choice. Nucleic Acids Research, 22, 4673-4680.
[25] Tamura, K., Stecher, G., Peterson, D., et al. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. The Society for Molecular Biology and Evolution, Oxford University, Oxford.
[26] Saitou, N. and Nei, M. (1987) The Neighbour-Joining Method: A New Method for Reconstructing Phylogenetic Trees. Molecular Phylogenetics and Evolution, 4, 406-425.
[27] Kimura, M. (1980) A Simple Method for Estimating Evolutionary Rates of Base Substitutions through Comparative Studies of Nucleotide Sequences. Applied and Environmental Microbiology, 16, 111-120.
[28] Siddiquee, S., Esmarada, A.K.W. and Abdullah, F. (2010) The Taxonomic Identity of Termitomyces aurantiacus by Using the Internal Transcribed Spacers 1 and 2 Regions of the rDNA. Mycology and Plant Pathology Lab, Department of Biology, University Putra Malaysia, UPM Serdang.
[29] You, Y.H., Yoon, H., Kang, S.M., et al. (2013) Cadophora malorum Cs-8-1 as a New Fungal Strain Producing Gibberellins Isolated from Calystegia soldanella. Journal of Basic Microbiology, 53, 630-634.
[30] He, Y., Tian, Y., Ye, R. and Ma, L. (2011) Isolation, Characterization and Antimicrobial Activity of Endophytic Fungi from Polygonum cuspidatum Sieb. et Zucc. School of Chemical Engineering, Sichuan University, Chengdu.
[31] Ju, Y.M. and Hsieh, H.M. (2007) Xylaria Species Associated with Nests of Oontotermes formosanus in Taiwan. Mycology, 99, 936-957.
[32] Hsieh, H.M., Lin, C.R., Fang, M.J., Rogers, J.D., Fournier, J., Lechat, C. and Ju, Y.-M. (2010) Phylogenetic Status of Xylaria subgenus Pseudoxylaria among Taxa of the Subfamily Xylarioideae (Xylariaceae) and Phylogeny of the Taxa Involved in the Subfamily. Molecular Phylogenetics and Evolution, 54, 957-969.
[33] Reddy, S.M., Suryanarayanan, T.S., Aggarwal, A. and Babu, G.A. (2010) Endophytic Xylariaceae of Western Ghats, Southern India: Diversity and Bioactive Compounds. Department of Biotechnology, Thapar University, Patiala.
[34] Restrepo, S., Avila, L., Lopera, C., et al. (2007) Fungal Endophytes from an Andean Colombian Paramo Ecosystem Inhibit the in Vitro Growth of Plant Pathogens. Biological Sciences, Los Andes University, Bogota.
[35] Sanmee, R., Dell, B., Lumyong, P. and Lumyong, S. (2007) First Record of Tricholoma fulvocastaneum from Thailand. Mycoscience, 48, 131-133.
[36] Sabotic, J., Gaser, D., Rogelj, B., Gruden, K., Strukelj, B. and Brzin, J. (2006) Heterogeneity in the Cysteine Protease Inhibitor Clitocypin Gene Family. Biological Chemistry, 387, 1559-1566.
[37] Nobre, T., Eggleton, P. and Aanen, D.K. (2010) Vertical Transmission as the Key to the Colonization of Madagascar by Fungus-Growing Termites? Proceedings of the Royal Society B: Biological Sciences, 277, 359-365.
[38] Rouland-Lefevre, C., Diouf, M.N., Brauman, A. and Neyra, M. (2002) Phylogenetic Relationships in Termitomyces (Family Agaricaceae) Based on the Nucleoticle Sequence of ITS: A First Approach to Elucidate the Evolutionary History of the Symbiosis between Fungus-Growing Termites and Their Fungi. Molecular Phylogenetics and Evolution, 22, 423-429.
[39] Sands, W.A. (1969) The Association of Termites and Fungi. In: Krishna, K. and Weesner, F.M., Eds., Biology of Termites, Academic Press, London, 495-524.
[40] Davet, P. and Rouxel, F. (1997) Détection et isolement des champignons du sol. INRA, Paris, 203 p.
[41] Osiemo, Z.B., Marten, A., Kaib, M., Gitonga, L.M., Boga, H.I. and Brandl, R. (2010) Open Relationships in the Castles of Clay: High Diversity and Low Host Specificity of Termitomyces Fungi Associated with Fungus-Growing Termites in Africa. Insectes Sociaux, 57, 351-363.
[42] Rogers, J.D., Ju, Y.M. and Lehmann, J. (2005) Some Xylaria Species on Termite Nests. Mycologiga, 97, 914-923.
[43] Shinzato, N., Muramatsu, M., Watanabe, Y. and Matsui, T. (2005) Termite-Regulated Fungal Monoculture in Fungus Combs of a Macrotermitine Termite Odontotermes formosanus. Zoological Science, 22, 917-922.
[44] Okane, I. and Nakagiri, A. (2007) Taxonomy of an Anamorphic Xylariaceous Fungus from a Termite Nest Found Together with Xylaria angulosa. Mycoscience, 48, 240-249.
[45] Sannasi, A. (1969) Possible Factor Responsible for Specific Growth of Xylaria nigripes in the Fungus Garden of the Mounds of the Termite Odontotermes redemanni. Entomologia experimentalis et applicata, 12, 183-190.
[46] Visser, A.A., Ros, V.I., De Beer, Z.W., Debets, A.J.M., Hartog, E., Kuyper, T.W., et al. (2009) Levels of Specificity of Xylaria Species Associated with Fungus-Growing Termites: A Phylogenetic Approach. Molecular Ecology, 18, 553-567.

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.