Abstract
A strain of the fungal genus Mariannaea, isolated from decayed leaves of Japanese red pine (Pinus densiflora), was identified to be a new species based on its molecular phylogeny and morphology. Molecular phylogenetic analysis revealed that the fungus belongs to a clade containing M. punicea and related species (M. punicea-related species) and that it forms a lineage independent of these species. Microscopic morphological comparisons with M. punicea-related species indicated that the new isolate differs with respect to the width of the phialides and length of the conidiophores. Comparison of macroscopic morphological characteristics revealed that M. punicea-related species are characterized by reddish-purple colonies, whereas the new isolate lacks this distinctive pigmentation. Moreover, the surface structure of the colonies of this fungus has a distinct irregular undulate pattern toward the margins. Given that this isolate can be clearly distinguished from the known M. punicea-related species, we consider the fungus to be a newly identified species, for which we propose the name Mariannaea imbricata sp. nov.
References
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Edler, D., Klein, J., Antonelli, A. & Silvestro, D. (2021) raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution 12: 373–377. https://doi.org/10.1111/2041-210X.13512
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Glass, N.L. & Donaldson, G.C. (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
Gräfenhan, T., Schroers, H.J., Nirenberg, H.I. & Seifert, K.A. (2011) An overview of the taxonomy, phylogeny and typification of some nectriaceous fungi classified in Cosmospora, Acremonium, Fusarium, Stilbella and Volutella. Studies in Mycology 68: 79–113. https://doi.org/10.3114/sim.2011.68.04
Hu, D.H., Wang, M. & Cai, L. (2017) Phylogenetic assessment and taxonomic revision of Mariannaea. Mycological Progress 16: 271–283. https://doi.org/10.1007/s11557-016-1252-2
Hyde, K.D., Dong, Y., Phookamsak, R., Jeewon, R., Bhat, D.J., Jones, E.B.G., Liu, N.G., Abeywickrama, P.D., Mapook, A., Wei, D., Perera, R.H., Manawasinghe, I.S., Pem, D., Bundhun, D., Karunarathna, A., Ekanayaka, A.H., Bao, D.F., Li, J., Samarakoon, M.C., Chaiwan, N., Lin, C.G., Phutthacharoen, K., Zhang, S.N., Senanayake, I.C., Goonasekara, I.D., Thambugala, K.M., Phukhamsakda, C., Tennakoon, D.S., Jiang, H.B., Yang, J., Zeng, M., Huanraluek, N., Liu, J.K., Wijesinghe, S.N., Tian, Q., Tibpromma, S., Brahmanage, R.S., Boonmee, S., Huang, S.K., Thiyagaraja, V., Lu, Y.Z., Jayawardena, R.S., Dong, W., Yang, E.F., Singh, S.K., Singh, S.M., Rana, S., Lad, S.S., Anand, G., Devadatha, B., Niranjan, M., Sarma, V.V., Liimatainen, K., Aguirre-Hudson, B., Niskanen, T., Overall, A., Alvarenga, R.L.M., Gibertoni, T.B., Pfliegler, W.P., Horváth, E., Imre, A., Alves, A.L., da Silva Santos, A.C., Tiago, P.V., Bulgakov, T.S., Wanasinghe, D.N., Bahkali, A.H., Doilom, M., Elgorban, A.M., Maharachchikumbura, S.S.N., Rajeshkumar, K.C., Haelewaters, D., Mortimer, P.E., Zhao, Q., Lumyong, S., Xu, J. & Sheng, J. (2020) Fungal diversity notes 1151–1276: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Diversity 100: 5–277. https://doi.org/10.1007/s13225-020-00439-5
Ishiuchi, K., Hirose, D., Kondo., Watanabe, K., Terasaka, K. & Makino, T. (2020) Mariannamides A and B, new cyclic octapeptides isolated from Mariannaea elegans NBRC102301. Bioorganic & Medicinal Chemistry Letters 30: 126946. https://doi.org/10.1016/j.bmcl.2019.126946
Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166. https://doi.org/10.1093/bib/bbx108
Kozlov, A.M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Lemoine, F., Domelevo Entfellner, J.B., Wilkinson, E., Correia, D., Dávila Felipe, M., De Oliveira, T. & Gascuel, O. (2018) Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556: 452–456. https://doi.org/10.1038/s41586-018-0043-0
Lombard, L., Van der Merwe, N.A., Groenewald, J.Z. & Crous, P.W. (2015) Generic concepts in Nectriaceae. Studies in Mycology 80: 189–245. http://dx.doi.org/10.1016/j.simyco.2014.12.002
Luangsa-ard, J.J., Hywel-Jones, N.L., Manoch, L. & Samson, R.A. (2005) On the relationships of Paecilomyces sect. Isarioidea species. Mycological Research 109 (05): 581–589. https://doi.org/10.1017/S0953756205002741
Matsushima, T. (1995) Matsushima Mycological Memoirs No. 8. Matsushima Fungus Collect, Kobe, Japan Murray, M.G. & Thompson, W.F. (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8: 4321–4326. https://doi.org/10.1093/nar/8.19.4321
Nonaka, K., Kaneta, T., Omura, S. & Masuma, R. (2015) Mariannaea macrochlamydospora, a new hyphomycete (Nectriaceae) from soil in the Bonin Islands, Japan. Mycoscience 56: 29–33. http://dx.doi.org/10.1016/j.myc.2014.02.001
O’Donnell, K. & Cigelink, E. (1997) Two divergent intragenomic rRNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution 7: 103–116. https://doi.org/10.1006/mpev.1996.0376
Ogawa, Y., Suda, A., Kusama-Eguchi, K., Watanabe, K. & Tokumasu, S. (2005) Intraspecific groups of Umbelopsis ramanniana inferred from nucleotide sequences of nuclear rDNA internal transcribed spacer regions and sporangiospore morphology. Mycoscience 46: 343–351. http://dx.doi.org/10.1007/s10267-005-0257-5
Okuda, T. & Yamamoto, K. (2000) Materials for the fungus flora of Japan (56) Mariannaea camptospora and M. elegans var. punicea from Japan. Mycoscience 41: 411–414. https://doi.org/10.1007/BF02463957
Samson, R.A. (1974) Paecilomyces and some allied hyphomycetes. Studies in Mycology 6: 1–117.
Samson, R.A. & Bigg, W.L. (1988) A new species of Mariannaea from California. Mycologia 80 (1): 131–134. https://doi.org/10.1080/00275514.1988.12025512
Samuels, G.J. (1989) Nectria and Penicillifer. Mycologia 81 (3): 347–355. https://doi.org/10.1080/00275514.1989.12025758
Shimazu, M. & Sato, H. (1996) Media for selective isolation of an entomogenous fungus, Beauveria bassiana (Deuteromycotina: Hyphomycetes). Applied Entomology and Zoology 31 (2): 291–298. https://doi.org/10.1303/aez.31.291
Tokumasu, S. (1996) Mycofloral succession on Pinus densiflora needles on a modern site. Mycoscience 37: 313–321. https://doi.org/10.1007/BF02461303
Vu, D., Groenewald, M., de Vries, M., Gehrmann, T., Stielow, B., Eberhardt, U., Al-Hatmi, A., Groenewald, J.Z., Cardinali, G., Houbraken, J., Boekhout, T., Crous, P.W., Robert, V. & Verkley, G.J.M. (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology 92: 135–154. https://doi.org/10.1016/j.simyco.2018.05.001
White, T.J., Bruns, T., Lee, S. & 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. & White, Y.J. (eds.) PCR Protocols: A Guide to Methods and Application. Academic Press, San Diego, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Zeng, Z.Q. & Zhuang, W.Z. (2014) A new holomorphic species of Mariannaea and epitypification of M. samuelsii. Mycological Progress 13: 967–973. https://doi.org/10.1007/s11557-014-0980-4
Crous, P.W., Wingfield, M.J., Lombard, L., Roets, F., Swart, W.J., Alvarado, P., Carnegie, A.J., Moreno, G., Luangsa-Ard, J., Thangavel, R., Alexandrova, A.V., Baseia, I.G., Bellanger, J.M., Bessette, A.E., Bessette, A.R., Delapeña-Lastra, S., García, D., Gené, J., Pham, T.H.G., Heykoop, M., Malysheva, E., Malysheva, V., Martín, M.P., Morozova, O.V., Noisripoom, W., Overton, B.E., Rea, A.E., Sewall, B.J., Smith, M.E., Smyth, C.W., Tasanathai, K., Visagie, C.M., Adam?ík, S., Alves, A., Andrade, J.P., Aninat, M.J., Araújo, R.V.B., Bordallo, J.J., Boufleur, T., Baroncelli, R., Barreto, R.W., Bolin, J., Cabero, J., Cabo?, M., Cafà, G., Caffot, M.L.H., Cai, L., Carlavilla, J.R., Chávez, R., Decastro, R.R.L., Delgat, L., Deschuyteneer, D., Dios, M.M., Domínguez, L.S., Evans, H.C., Eyssartier, G., Ferreira, B.W., Figueiredo, C.N., Liu, F., Fournier, J., Galli-Terasawa, L.V., Gil-Durán, C., Glienke, C., Gonçalves, M.F.M., Gryta, H., Guarro, J., Himaman, W., Hywel-Jones, N., Iturrieta-González, I., Ivanushkina, N.E., Jargeat, P., Khalid, A.N., Khan, J., Kiran, M., Kiss, L., Kochkina, G.A., Kola?ík, M., Kubátová, A., Lodge, D.J., Loizides, M., Luque, D., Manjón, J.L., Marbach, P.A.S., Massolajr, N.S., Mata, M., Miller, A.N., Mongkolsamrit, S., Moreau, P.A., Morte, A., Mujic, A., Navarro-Ródenas, A., Németh, M.Z., Nóbrega, T.F., Nováková, A., Olariaga, I., Ozerskaya, S.M., Palma, M.A., Petters-Vandresen, D.A.L., Piontelli, E., Popov, E.S., Rodríguez, A., Requejo, Ó., Rodrigues, A.C.M., Rong, I.H., Roux, J., Seifert, K.A., Silva, B.D.B., Sklená?, F., Smith, J.A., Sousa, J.O., Souza, H.G., Desouza, J.T., Švec, K., Tanchaud, P., Tanney, J.B., Terasawa, F., Thanakitpipattana, D., Torres-Garcia, D., Vaca, I., Vaghefi, N., Vaniperen, A.L., Vasilenko, O.V., Verbeken, A., Yilmaz, N., Zamora, J.C., Zapata, M., Jurjevi, Ž. & Groenewald, J.Z. (2019) Fungal Planet description sheets: 868–950. Persoonia 42: 291–473. https://doi.org/10.3767/persoonia
Darriba, D., Posada, D., Kozlov, A.M., Stamatakis, A., Morel, B. & Flouri, T. (2020) ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37: 291–294. https://doi.org/10.1093/molbev/msz189
Domsch, K.H., Grams, W. & Anderson, T.H. (2007) Compendium of soil fungi second edition. pp. 256–266.
Edler, D., Klein, J., Antonelli, A. & Silvestro, D. (2021) raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution 12: 373–377. https://doi.org/10.1111/2041-210X.13512
Fukuda, T., Sudoh, Y., Tsuchiya, Y., Okuda, T., Fujimori, F. & Igarashi, Y. (2011) Marianins A and B, prenylated phenylpropanoids from Mariannaea camptospora. Journal of Natural Products 74: 1327–1330. https://doi.org/10.1021/np200035m
Glass, N.L. & Donaldson, G.C. (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
Gräfenhan, T., Schroers, H.J., Nirenberg, H.I. & Seifert, K.A. (2011) An overview of the taxonomy, phylogeny and typification of some nectriaceous fungi classified in Cosmospora, Acremonium, Fusarium, Stilbella and Volutella. Studies in Mycology 68: 79–113. https://doi.org/10.3114/sim.2011.68.04
Hu, D.H., Wang, M. & Cai, L. (2017) Phylogenetic assessment and taxonomic revision of Mariannaea. Mycological Progress 16: 271–283. https://doi.org/10.1007/s11557-016-1252-2
Hyde, K.D., Dong, Y., Phookamsak, R., Jeewon, R., Bhat, D.J., Jones, E.B.G., Liu, N.G., Abeywickrama, P.D., Mapook, A., Wei, D., Perera, R.H., Manawasinghe, I.S., Pem, D., Bundhun, D., Karunarathna, A., Ekanayaka, A.H., Bao, D.F., Li, J., Samarakoon, M.C., Chaiwan, N., Lin, C.G., Phutthacharoen, K., Zhang, S.N., Senanayake, I.C., Goonasekara, I.D., Thambugala, K.M., Phukhamsakda, C., Tennakoon, D.S., Jiang, H.B., Yang, J., Zeng, M., Huanraluek, N., Liu, J.K., Wijesinghe, S.N., Tian, Q., Tibpromma, S., Brahmanage, R.S., Boonmee, S., Huang, S.K., Thiyagaraja, V., Lu, Y.Z., Jayawardena, R.S., Dong, W., Yang, E.F., Singh, S.K., Singh, S.M., Rana, S., Lad, S.S., Anand, G., Devadatha, B., Niranjan, M., Sarma, V.V., Liimatainen, K., Aguirre-Hudson, B., Niskanen, T., Overall, A., Alvarenga, R.L.M., Gibertoni, T.B., Pfliegler, W.P., Horváth, E., Imre, A., Alves, A.L., da Silva Santos, A.C., Tiago, P.V., Bulgakov, T.S., Wanasinghe, D.N., Bahkali, A.H., Doilom, M., Elgorban, A.M., Maharachchikumbura, S.S.N., Rajeshkumar, K.C., Haelewaters, D., Mortimer, P.E., Zhao, Q., Lumyong, S., Xu, J. & Sheng, J. (2020) Fungal diversity notes 1151–1276: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Diversity 100: 5–277. https://doi.org/10.1007/s13225-020-00439-5
Ishiuchi, K., Hirose, D., Kondo., Watanabe, K., Terasaka, K. & Makino, T. (2020) Mariannamides A and B, new cyclic octapeptides isolated from Mariannaea elegans NBRC102301. Bioorganic & Medicinal Chemistry Letters 30: 126946. https://doi.org/10.1016/j.bmcl.2019.126946
Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166. https://doi.org/10.1093/bib/bbx108
Kozlov, A.M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Lemoine, F., Domelevo Entfellner, J.B., Wilkinson, E., Correia, D., Dávila Felipe, M., De Oliveira, T. & Gascuel, O. (2018) Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556: 452–456. https://doi.org/10.1038/s41586-018-0043-0
Lombard, L., Van der Merwe, N.A., Groenewald, J.Z. & Crous, P.W. (2015) Generic concepts in Nectriaceae. Studies in Mycology 80: 189–245. http://dx.doi.org/10.1016/j.simyco.2014.12.002
Luangsa-ard, J.J., Hywel-Jones, N.L., Manoch, L. & Samson, R.A. (2005) On the relationships of Paecilomyces sect. Isarioidea species. Mycological Research 109 (05): 581–589. https://doi.org/10.1017/S0953756205002741
Matsushima, T. (1995) Matsushima Mycological Memoirs No. 8. Matsushima Fungus Collect, Kobe, Japan Murray, M.G. & Thompson, W.F. (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8: 4321–4326. https://doi.org/10.1093/nar/8.19.4321
Nonaka, K., Kaneta, T., Omura, S. & Masuma, R. (2015) Mariannaea macrochlamydospora, a new hyphomycete (Nectriaceae) from soil in the Bonin Islands, Japan. Mycoscience 56: 29–33. http://dx.doi.org/10.1016/j.myc.2014.02.001
O’Donnell, K. & Cigelink, E. (1997) Two divergent intragenomic rRNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution 7: 103–116. https://doi.org/10.1006/mpev.1996.0376
Ogawa, Y., Suda, A., Kusama-Eguchi, K., Watanabe, K. & Tokumasu, S. (2005) Intraspecific groups of Umbelopsis ramanniana inferred from nucleotide sequences of nuclear rDNA internal transcribed spacer regions and sporangiospore morphology. Mycoscience 46: 343–351. http://dx.doi.org/10.1007/s10267-005-0257-5
Okuda, T. & Yamamoto, K. (2000) Materials for the fungus flora of Japan (56) Mariannaea camptospora and M. elegans var. punicea from Japan. Mycoscience 41: 411–414. https://doi.org/10.1007/BF02463957
Samson, R.A. (1974) Paecilomyces and some allied hyphomycetes. Studies in Mycology 6: 1–117.
Samson, R.A. & Bigg, W.L. (1988) A new species of Mariannaea from California. Mycologia 80 (1): 131–134. https://doi.org/10.1080/00275514.1988.12025512
Samuels, G.J. (1989) Nectria and Penicillifer. Mycologia 81 (3): 347–355. https://doi.org/10.1080/00275514.1989.12025758
Shimazu, M. & Sato, H. (1996) Media for selective isolation of an entomogenous fungus, Beauveria bassiana (Deuteromycotina: Hyphomycetes). Applied Entomology and Zoology 31 (2): 291–298. https://doi.org/10.1303/aez.31.291
Tokumasu, S. (1996) Mycofloral succession on Pinus densiflora needles on a modern site. Mycoscience 37: 313–321. https://doi.org/10.1007/BF02461303
Vu, D., Groenewald, M., de Vries, M., Gehrmann, T., Stielow, B., Eberhardt, U., Al-Hatmi, A., Groenewald, J.Z., Cardinali, G., Houbraken, J., Boekhout, T., Crous, P.W., Robert, V. & Verkley, G.J.M. (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology 92: 135–154. https://doi.org/10.1016/j.simyco.2018.05.001
White, T.J., Bruns, T., Lee, S. & 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. & White, Y.J. (eds.) PCR Protocols: A Guide to Methods and Application. Academic Press, San Diego, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Zeng, Z.Q. & Zhuang, W.Z. (2014) A new holomorphic species of Mariannaea and epitypification of M. samuelsii. Mycological Progress 13: 967–973. https://doi.org/10.1007/s11557-014-0980-4