Abstract
A new entomopathogenic fungus in the genus Ophiocordyceps from Southwestern China, is described and illustrated here under the name Ophiocordyceps anshunensis. It is characterized by 30-80 mm long stromata with smaller (2.4–5.0 × 1.2–2.8 mm) oval to ellipse shaped fertile head and 8.3−17.6 × 1.1–2.0 µm part-spores. According to phylogenetic analyses of combined ITS, LSU, TEF, RPB1, and RPB2 sequences, the new species is sister to O. nutans, from which differ by the aforementioned characteristics. A tabular comparison between the new species and related and similar taxa is provided.
References
- Araújo, J.P. & Hughes, D.P. (2019) Zombie-ant fungi emerged from non-manipulating, beetle-infecting ancestors. Current Biology 29: 3735–3738. https://doi.org/10.1016/j.cub.2019.09.004
- 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/10.1007/s11557-014-1017-8
- Bischoff, J.F., Rehner, S.A. & Humber, R.A. (2006) Metarhizium frigidum sp. nov.: a cryptic species of M. anisopliae and a member of the M. flavoviride complex. Mycologia 98: 737–745. https://doi.org/10.3852/mycologia.98.5.737
- Blossey, B. & Hunt-Joshi, T.R. (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annual Review of Entomology 48: 521–547. https://doi.org/10.1146/annurev.ento.48.091801.112700
- Chen, W., Zhang, W., Shen, W. & Wang, K. (2010) Effects of the acid polysaccharide fraction isolated from a cultivated Cordyceps sinensis on macrophages in vitro. Cellular Immunology 262: 69–74. https://doi.org/10.1016/j.cellimm.2010.01.001
- Conti, E., Avila, G., Barratt, B., Cingolani, F., Colazza, S., Guarino, S., Hoelmer, K., Laumann, R.A., Maistrello, L., Martel, G. & Peri, E. (2021) Biological control of invasive stink bugs: review of global state and future prospects. Entomologia Experimentalis et Applicata 169: 28–51. https://doi.org/10.1111/eea.12967
- Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109
- Friedrich, R.C.S., Shrestha, B., Salvador-Montoya, C., Tomé, L.M., Reck, M., Góes-Neto, A. & Drechsler-Santos, E. (2018) Ophiocordyceps neonutans sp. nov., a new neotropical species from O. nutans complex (Ophiocordycipitaceae, Ascomycota). Phytotaxa 344 (3): 215–227. https://doi.org/10.11646/phytotaxa.344.3.2
- He, L., Ji, P., Cheng, J., Wang, Y., Qian, H., Li, W., Gong, X. & Wang, Z. (2013) Structural characterization and immunostimulatory activity of a novel protein-bound polysaccharide produced by Hirsutella sinensis Liu, Guo, Yu & Zeng. Food Chemistry 141: 946–953. https://doi.org/10.1016/j.foodchem.2013.04.053
- Henry, T.J. (2017) Biodiversity of heteroptera. Insect Biodiversity: science and society 21: 279–335. https://doi.org/10.1002/9781118945568.ch10
- Hyde, K.D., Chaiwan, N., Norphanphoun, C., Boonmee, S., Camporesi, E., Chethana, K.W.T., Dayarathne, M.C., De Silva, N.I., Dissanayake, A.J., Ekanayaka, A.H. & Hongsanan, S. (2018) Mycosphere notes 169–224. Mycosphere 9: 271–430. https://doi.org/10.5943/mycosphere/9/2/8
- Hyde, K.D., Hongsanan, S., Jeewon, R., Bhat, D.J., McKenzie, E.H.C., Jones, E.B.G., Phookamsak, R., Ariyawansa, H.A., Boonmee, S., Zhao, Q., Abdel-Aziz, F.A., Abdel-Wahab, M.A., Banmai, S., Chomnunti, P., Cui, B.K., Daranagama, D.A., Das, K., Dayarathne, M.C., de Silva, N.I., Dissanayake, A.J., Doilom, M., Ekanayaka, A.H., Gibertoni, T.B., Góes-Neto, A., Huang, S.K., Jayasiri, S.C., Jayawardena, R.S., Konta, S., Lee, H.B., Li, W.J., Lin, C.G., Liu, J.K., Lu, Y.Z., Luo, Z.L., Manawasinghe, I.S., Manimohan, P., Mapook, A., Niskanen, T., Norphanphoun, C., Papizadeh, M., Perera, R.H., Phukhamsakda, C., Richter, C., de A. Santiago, A.L.C.M., Drechsler-Santos, E.R., Senanayake, I.C., Tanaka, K., Tennakoon, T.M.D.S., Thambugala, K.M., Tian, Q., Tibpromma, S., Thongbai, B., Vizzini, A., Wanasinghe, D.N., Wijayawardene, N.N., Wu, H.X., Yang, J., Zeng, X.Y., Zhang, H., Zhang, J.F., Bulgakov, T.S., Camporesi, E., Bahkali, A.H., Amoozegar, M.A., Araujo-Neta, L.S., Ammirati, J.F., Baghela, A., Bhatt, R.P., Bojantchev, D., Buyck, B., da Silva, G.A., de Lima, C.L.F., de Oliveira, R.J.V., de Souza, C.A.F., Dai, Y.C., Dima, B., Duong, T.T., Ercole, E., Mafalda-Freire, F., Ghosh, A., Hashimoto, A., Kamolhan, S., Kang, J.C., Karunarathna, S.C., Kirk, P.M., Kytövuori, I., Lantieri, A., Liimatainen, K., Liu, Z.Y., Liu, X.Z., Lücking, R., Medardi, G., Mortimer, P.E., Nguyen, T.T.T., Promputtha, I., Raj, K.N.A., Reck, M.A., Lumyong, S., Shahzadeh-Fazeli, S.A., Stadler, M., Soudi, M.R., Su, H.Y., Takahashi, T., Tangthirasunun, N., Uniyal, P., Wang, Y., Wen, T.C., Xu, J.C., Zhang, Z.K., Zhao, Y.C., Zhou, J.L. & Zhu, L. (2016) Fungal diversity notes 367–490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity 80: 1–270. https://doi.org/10.1007/s13225-016-0373-x
- Khao-Ngam, S., Mongkolsamrit, S., Rungjindamai, N., Noisripoom, W., Pooissarakul, W., Duangthisan, J., Himaman, W. & Luangsa-Ard, J.J. (2021) Ophiocordyceps asiana and Ophiocordyceps tessaratomidarum (Ophiocordycipitaceae, Hypocreales), two new species on stink bugs from Thailand. Mycological Progres 20: 341–353. https://doi.org/10.1007/s11557-021-01684-x
- Khonsanit, A., Luangsa-Ard, J.J., Thanakitpipattana, D., Kobmoo, N. & Piasai, O. (2019) Cryptic species within Ophiocordyceps myrmecophila complex on formicine ants from Thailand. Mycological Progress 18: 147–161. https://doi.org/10.1007/s11557-018-1412-7
- Lanfear, R., Calcott, B., Ho, S.Y. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29: 1695–1701. https://doi.org/10.1093/molbev/mss020
- Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. & Thompson, J.D. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948. https://doi.org/10.1093/bioinformatics/btm404
- Long, F.Y., Qin, L.W., Xiao, Y.P., Hyde ,K.D., Wang, S.X. & Wen, T.C. (2021) Multigene phylogeny and morphology reveal a new species, Ophiocordyceps vespulae, from Jilin Province, China. Phytotaxa 478: 33–48. https://doi.org/10.11646/phytotaxa.280.2.4
- Luangsa-Ard, J.J., Ridkaew, R., Tasanathai, K., Thanakitpipattana, D. & Hywel-Jones, N. (2011) Ophiocordyceps halabalaensis: a new species of Ophiocordyceps pathogenic to Camponotus gigas in Hala Bala Wildlife Sanctuary, Southern Thailand. Fungal Biology 115: 608–614. https://doi.org/10.1016/j.funbio.2011.03.002
- Meng, L.Z., Feng, K., Wang, L.Y., Cheong, K.L., Nie, H., Zhao, J. & Li, S.P. (2014) Activation of mouse macrophages and dendritic cells induced by polysaccharides from a novel Cordyceps sinensis fungus UM01. Journal of Functional Foods 9: 242–253. https://doi.org/10.1016/j.jff.2014.04.029
- Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., Von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37: 1530–1534. https://doi.org/10.1093/molbev/msaa015
- 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
- Quandt, C.A., Kepler, R.M., Gams, W., Araújo, J.P., Ban, S., Evans, H.C., Hughes, D., Humber, R., Hywel-Jones, N., Li, Z. & Luangsa-Ard, J.J. (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. & Buckley, E. (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97: 84–98. https://doi.org/10.3852/mycologia.97.1.84
- 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
- Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, 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
- Sanjuan, T.I., Franco-Molano, A.E., Kepler, R.M., Spatafora, J.W., Tabima, J., Vasco-Palacios, A.M. & Restrepo, S. (2015) Five new species of entomopathogenic fungi from the Amazon and evolution of neotropical Ophiocordyceps. Fungal Biology 119: 901–916. https://doi.org/10.1016/j.funbio.2015.06.010
- Sasaki, F., Miyamoto, T., Yamamoto, A., Tamai, Y. & Yajima, T. (2008) Morphological and genetic characteristics of the entomopathogenic fungus Ophiocordyceps nutans and its host insects. Mycological Research 112: 1241–1244. https://doi.org/10.1016/j.mycres.2008.04.008
- Schaefer, C.W. (2009) Prosorrhyncha: Heteroptera and Coleorrhyncha. Encyclopedia of Insects 839–855. https://doi.org/10.1016/B978-0-12-374144-8.00220-4
- Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., Chen, W., Crous, P.W., Boekhout, T., Damm, U., de Hoog, G.S., Eberhardt, U., Groenewald, J.Z., Groenewald, M., Hagen, F., Houbraken, J., Quaedvlieg, W., Stielow, B., Vu, T.D. & Walther, G. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences 109: 6241–6246. https://doi.org/10.1073/pnas.1117018109
- 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
- Spatafora, J.W., Sung, G.H., Sung, J.M., Hywel‐Jones, N.L. & White Jr, J.F. (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Molecular Ecology 16: 1701–1711. https://doi.org/10.1111/j.1365-294X.2007.03225.x
- Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57: 758–771. https://doi.org/10.1080/10635150802429642
- 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
- Sung, J.M., Kim, C.H., Yang, K.J., Lee, H.K. & Kim, Y.S. (1993) Studies on distribution and utilization of Cordyceps militaris and C. nutans. Korean Journal of Mycology 21: 94–105.
- Swofford, D.L. (2002) Phylogenetic analysis using parsimony (* and other methods). Version 4: b10. https://doi.org/10.1111/j.0014-3820.2002.tb00191.x
- Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197
- Tillman, G. (2008) Populations of stink bugs (Heteroptera: Pentatomidae) and their natural enemies in peanuts. Journal of Entomological Science 43: 191–207. https://doi.org/10.18474/0749-8004-43.2.191
- Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cyptococcus species. Journal of Bacteriology 172: 4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
- Wang, X.L. & Yao, Y.J. (2011) Host insect species of Ophiocordyceps sinensis: a review. ZooKeys 127: 43–59. https://doi.org/10.3897/zookeys.127.802
- Wang, Y., Dai, Y.D., Yang, Z.L., Guo, R., Wang, Y.B., Yang, Z.L., Ding, L. & Yu, H. (2021) Morphological and molecular phylogenetic data of the Chinese medicinal fungus Cordyceps liangshanensis reveal its new systematic position in the family Ophiocordycipitaceae. Mycobiology 49: 297–307. https://doi.org/10.1080/12298093.2021.1923388
- 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 Progres 17: 745–753. https://doi.org/10.1007/s11557-017-1370-5
- Wei, D.P., Gentekaki, E., Wanasinghe, D.N., Tang, S.M. & Hyde, K.D. (2022) Diversity, molecular dating and ancestral characters state reconstruction of entomopathogenic fungi in Hypocreales. Mycosphere 13: 281–351. https://doi.org/10.5943/mycosphere/si/1f/8
- Wei, D.P., Wanasinghe, D.N., Hyde, K.D., Mortimer, P.E., Xu, J.C., To-Anun, C., Yu, F.M. & Zha, L.S. (2020) Ophiocordyceps tianshanensis sp. nov. on ants from Tianshan mountains, PR China. Phytotaxa 464 (4): 277–292. https://doi.org/10.11646/phytotaxa.464.4.2
- White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) 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 18: 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
- Wijayawardene, N.N., Hyde, K.D., Rajeshkumar, K.C., Hawksworth, D.L., Madrid, H., Kirk, P.M., Braun, U., Singh, R.V., Crous, P.W., Kukwa, M. & Luecking, R. (2017) Notes for genera: Ascomycota. Fungal Diversity 86: 1–594. https://doi.org/10.1007/s13225-017-0386-0
- Wu, D.T., Meng, L.Z., Wang, L.Y., Lv, G.P., Cheong, K.L., Hu, D.J., Guan, J., Zhao, J. & Li, S.P. (2014) Chain conformation and immunomodulatory activity of a hyperbranched polysaccharide from Cordyceps sinensis. Carbohydrate Polymers 110: 405–414. https://doi.org/10.1016/j.carbpol.2014.04.044
- Xiao, Y.P., Hongsanan, S., Hyde, K.D., Brooks, S., Xie, N., Long, F.Y. & Wen, T.C. (2019) Two new entomopathogenic species of Ophiocordyceps in Thailand. MycoKeys 47: 53–74. https://doi.org/10.3897/mycokeys.47.29898
- Xiao, Y.P., Wen, T.C., Hongsanan, S., Sun, J.Z. & Hyde, K.D. (2017) Introducing Ophiocordyceps thanathonensis, a new species of entomogenous fungi on ants, and a reference specimen for O. pseudolloydii. Phytotaxa 328: 115–126. https://doi.org/10.11646/phytotaxa.328.2.2
- Yang, Y., Xiao, Y.P., Yu ,G., Wen, T., Deng, C., Meng, J. & Lu, Z. (2021) Ophiocordyceps aphrophoridarum sp. nov., a new entomopathogenic species from Guizhou, China. Biodiversity Data Journal 9: 1–13. https://doi.org/10.3897/BDJ.9.e66115
- Zucchi, M.I., Cordeiro, E.M., Wu, X., Lamana, L.M., Brown, P.J., Manjunatha, S., Viana, J.P.G., Omoto, C., Pinheiro, J.B. & Clough, S.J. (2019) Population genomics of the Neotropical brown stink bug, Euschistus heros: the most important emerging insect pest to soybean in Brazil. Frontiers in Genetics 10: 35. https://doi.org/10.3389/fgene.2019.01035