Abstract
Ophiocordyceps is an entomopathogenic fungal genus with global distribution and considerable economic implications in both biological control and biomedicine. However, the species diversity of Ophiocordyceps remains to be further investigated. In this study, a new species, Ophiocordyceps xifengensis, found parasitizing lepidopteran pupae, was discovered during a survey of insect pathogenic fungi in Xifeng County, Liaoning Province. Morphological comparative analysis revealed that this species characterized by having solitary, non-branching, woody, cylindrical asci and filamentous ascospores. Compared to its closely related species, the new species exhibits inclined embedded perithecia (0.38–0.43 mm) and smaller asci (164.8–178.9 × 7.4–10.2 μm), with its anamorphic features. Phylogenetic analysis based on multiple gene sequence data infers that Ophiocordyceps xifengensis, forming a distinct branch from other closely related species.
References
- Anisimova, M., Gil, M., Dufayard, J.F., Dessimoz, C. & Gascuel, O. (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast Likelihood-based approximation schemes. Systematic Biology 60: 685–699.
- https://doi.org/10.1093/sysbio/syr041
- Ban, S., Sakane, T. & Nakagiri, A. (2015) Three new species of Ophiocordyceps and overview of anamorph types in the genus and the family Ophiocordyceptaceae. Mycological Progress 14: 1–12.
- https://doi.org/ARTN 101710.1007/s11557–014–1017–8
- Castlebury, L.A., Rossman, A.Y., Gi-Ho, S., Hyten, A.S. & Spatafora, J.W. (2004) Multigene phylogeny reveals new lineage for Stachybotrys chartarum, the indoor air fungus. Mycological research 108: 864–872.
- https://doi.org/10.1017/s0953756204000607
- Chen, Y.P., Su, P.W., Hyde, K.D. & Maharachchikumbura, S.S.N. (2023) Phylogenomics and diversification of Sordariomycetes. MYCOSPHERE 14(1): 414–451.
- https://doi.org/10.5943/mycosphere/14/1/5
- Evans, H.C. & Samson, R.A. (1982) Cordyceps species & their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems I. The Cephalotes (Myrmicinae) complex. Transactions of the British Mycological Society 79: 431–453.
- https://doi.org/10.1016/s0007–1536(82)80037–5
- Evans, H.C. & Samson, R.A. (1984) Cordyceps species & their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems II. The Camponotus (Formicinae) complex. Transactions of the British Mycological Society 82: 127–150.
- https://doi.org/10.1016/s0007–1536(84)80219–3
- Fan, Q., Wang, Y.B., Zhang, G.D., Tang, D.X. & Yu, H. (2021) Multigene phylogeny & morphology of Ophiocordyceps alboperitheciata sp. nov., A new entomopathogenic fungus attacking lepidopteran larva from Yunnan, China. Mycobiology 49: 133–141.
- https://doi.org/10.1080/12298093.2021.1903130
- Gomez‐Polo, P., Ballinger, M.J., Lalzar, M., Malik, A., Ben‐Dov, Y., Mozes‐Daube, N., Perlman, S.J., Iasur‐Kruh, L. & Chiel, E. (2017) An exceptional family: Ophiocordyceps‐allied fungus dominates the microbiome of soft scale insects (Hemiptera: Sternorrhyncha: Coccidae). Molecular Ecology 26: 5855–5868.
- https://doi.org/10.1111/mec.14332
- Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589.
- https://doi.org/10.1038/Nmeth.4285
- Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.
- https://doi.org/10.1093/molbev/mst010
- Kobayasi, Y. (1941) The genus Cordyceps and its allies. Science Reports of the Tokyo Bunrika Daigaku 84: 53–260.
- Kobayasi, Y. (1982) Keys to the taxa of the genera Cordyceps and Torrubiella. Transactions of the Mycological Society of Japan 23: 329–364.
- Liang, Z.Q., Liu, A.Y. & Huang, J.Z. (2005) Some entomogenous fungi from Wuyishan and Zhangjiajie nature reserves I. Cordyceps. Mycosystema 21: 162–166. [in Chinese]
- https://doi.org/10.1007/s11769-002-0037-5
- Liang, Z.Q. (1990) Studies on classification of the genus Hirsutella Pat. I. Advances and the characteristics of taxonomy. Journal of Guizhou Agricultural College 9: 58–68. [in Chinese]
- Luangsa-ard, J.J., Tasanathai, K., Thanakitpipattana, D., Khonsanit, A. & Stadler, M. (2018) Novel and interesting Ophiocordyceps spp. (Ophiocordycipitaceae, Hypocreales) with superficial perithecia from Thailand. Studies in Mycology 89: 125–142.
- https://doi.org/10.1016/j.simyco.2018.02.001
- Mains, E. (1958) North American entomogenous species of Cordyceps. Mycologia 50: 169–222.
- https://doi.org/10.1080/00275514.1958.12024722
- Mains, E.B. (1951) Entomogenous Species of Hirsutella, Tilachlidium and Synnematium. Mycologia 43: 691–718.
- https://doi.org/10.1080/00275514.1951.12024164
- Mongkolsamrit, S., Noisripoom, W., Arnamnart, N., Lamlertthon, S., Himaman, W., Jangsantear, P., Samson, R.A. & Luangsa-ard, J.J. (2019) Resurrection of Paraisaria in the Ophiocordycipitaceae with three new species from Thailand. Mycological Progress 18: 1213–1230.
- https://doi.org/10.1007/s11557-019-01518-x
- Nguyen, L.T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Molecular Biology and Evolution 32: 268–274.
- https://doi.org/10.1093/molbev/msu300
- Petch, T. (1931) Notes on entomogenous fungi. (At the University Press). Transactions of the British Mycological Society 16(1): 55–75.
- https://doi.org/10.1016/S0007-1536(31)80006-3
- Petch, T. (1935) Notes on entomogenous fungi. Transactions of the British Mycological Society 19(3): 161–194.
- https://doi.org/10.1016/s0007-1536(35)80008-9
- Petch, T. (1937) Notes on entomogenous fungi. Transactions of the British Mycological Society 21(1–2): 34–67.
- https://doi.org/10.1016/s0007-1536(37)80005-4
- Qu J.J., Yu L.Q., Zhang J., Han Y.F. & Zou, X. (2018) A new entomopathogenic fungus, Ophiocordyceps ponerus sp nov., from China. Phytotaxa 343(2): 116–126.
- https://doi.org/10.11646/phytotaxa.343.2.2
- Qu, J.J., Zou, X., Cao, W., Xu, Z.S. & Liang, Z.Q. (2021) Two new species of Hirsutella (Ophiocordycipitaceae, Sordariomycetes) that are parasitic on lepidopteran insects from China. Mycokeys 82: 81–96.
- https://doi.org/10.3897/mycokeys.82.66927
- Quandt, C.A., Kepler, R.M., Gams, W., Araujo, J.P.M., Ban, S., Evans, H.C., Hughes, D., Humber, R., Hywel-Jones, N., Li, Z.Z., Luangsa-ard, J.J., Rehner, S.A., Sanjuan, T., Sato, H., Shrestha, B., Sung, G.H., Yao, Y.J., Zare, R. & Spatafora, J.W. (2014) Phylogenetic-based nomenclatural proposals for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium. Ima Fungus 5: 121–134.
- https://doi.org/10.5598/imafungus.2014.05.01.12
- Rehner, S.A. & Samuels, G.J. (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycological Research 98: 625–634.
- https://doi.org/10.1016/s0953-7562(09)80409-7
- Rehner, S.A. & Buckley, E. (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1– sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97: 84–98.
- https://doi.org/10.3852/mycologia.97.1.84
- Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Systematic Biology 61: 539–542.
- https://doi.org/10.1093/sysbio/sys029
- Shrestha, B., Tanaka, E., Hyun, M.W., Han, J.-G., Kim, C.S., Jo, J.W., Han, S.-K., Oh, J. & Sung, G.-H. (2016) Coleopteran and Lepidopteran Hosts of the Entomopathogenic Genus Cordyceps sensu lato. Journal of Mycology 2016: 1–14.
- https://doi.org/10.1155/2016/7648219
- Simmons, D.R., Kepler, R.M., Rehner, S.A. & Groden, E. (2015a) Phylogeny of Hirsutella species (Ophiocordycipitaceae) from the USA: remedying the paucity of Hirsutella sequence data. Ima Fungus 6: 345–356.
- https://doi.org/10.5598/imafungus.2015.06.02.06
- Simmons, D.R., Lund, J., Levitsky, T. & Groden, E. (2015b) Ophiocordyceps myrmicarum, a new species infecting invasive Myrmica rubra in Maine. Journal of Invertebrate Pathology 125: 23–30.
- https://doi.org/10.1016/j.jip.2014.12.010
- Speare, A. (1920) On certain entomogenous fungi. Mycologia 12: 62–76.
- Sung, G.H., Hywel-Jones, N.L., Sung, J.M., Luangsa-ard, J.J., Shrestha, B. & Spatafora, J.W. (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology 57: 5–59.
- https://doi.org/10.3114/sim.2007.57.01
- Tasanathai, K., Noisripoom, W., Chaitika, T., Khonsanit, A., Hasin, S. & Luangsa-ard, J. (2019) Phylogenetic and morphological classification of Ophiocordyceps species on termites from Thailand. Mycokeys 56: 101–129.
- https://doi.org/10.3897/mycokeys.56.37636
- Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246.
- https://doi.org/10.1128/jb.172.8.4238-4246.1990
- Wang, Y.B., Wang, Y., Fan, Q., Duan, D. E., Zhang, G.D., Dai, R. Q., Dai, Y.D., Zeng, W.B., Chen, Z.H., Li, D.D., Tang, D. X., Xu, Z. H., Sun, T., Nguyen, T. T., Tran, N. L., Dao, V. M., Zhang, C. M., Huang, L. D., Liu, Y. J., Zhang, X. M., Yang, D. R., Sanjuan, T., Liu, X. Z., Yang, Z.L. & Yu, H. (2020) Multigene phylogeny of the family Cordycipitaceae (Hypocreales): new taxa and the new systematic position of the Chinese cordycipitoid fungus Paecilomyces hepiali. Fungal Diversity 103: 1–46.
- https://doi.org/10.1007/s13225-020-00457-3
- Wang, Y.B., Yu H., Dai Y.D., Chen Z.H., Zeng W.B., Yuan F. & Liang, Z.Q. (2015) Polycephalomyces yunnanensis (Hypocreales), a new species of Polycephalomyces parasitizing Ophiocordyceps nutans and stink bugs (hemipteran adults). Phytotaxa 208(1): 34–44.
- https://doi.org/10.11646/phytotaxa.208.1.3
- Wang, Y.B., Nguyen, T.T., Dai, Y.D., Yu, H., Zeng, W.B. & Wu, C.K. (2018) Molecular phylogeny and morphology of Ophiocordyceps unituberculata sp nov (Ophiocordycipitaceae), a pathogen of caterpillars (Noctuidae, Lepidoptera) from Yunnan, China. Mycological Progress 17: 745–753.
- https://doi.org/10.1007/s11557-017-1370-5
- White, T.J., Bruns, T.D., Lee, S.B. & Taylor, J.W. (1990) 38 - Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.), PCR protocols: a guide to methods and applications. Academic Press, New York, pp. 315–322.
- https://doi.org/10.1016/B978-0-12-372180-8.50042-1
- Xiang, C.‐Y., Gao, F.-H., Jakovlić, I., Lei, H.-P., Hu, Y., Zhang, H., Zou, H., Wang, G.-T. & Zhang, D. (2023) Using PhyloSuite for molecular phylogeny and tree‐based analyses. iMeta 2023: e87.
- https://doi.org/10.1002/imt2.87
- Zhang, D., Gao, F.L., Jakovlic, I., Zou, H., Zhang, J., Li, W.X. & Wang, G.T. (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20: 348–355.
- https://doi.org/10.1111/1755-0998.13096
- Zou, X, Zhou, Y.M., Liang, Z.Q. & Xu, F.L. (2016) A new species of the genus Hirsutella with helical twist neck of phialides parasitized on Tortricidae. Mycosystema 35: 807–813. [in Chinese]
- Zou, X, Zhou, J.X., Liang, Z.Q. & Han, Y.F. (2016) Hirsutella shennongjiaensis, a new entomopathogenic species infecting earwig (Dermaptera). Mycosystema 35: 1070–1079. [in Chinese]
- https://doi.org/10.13346/j.mycosystema.160077