Abstract
Paraisaria is distinct from Ophiocordyceps and is resurrected as a valid genus within Ophiocordycipitaceae. Multi-gene phylogenetic analyses and morphological characterization support the split of Paraisaria from Ophiocordyceps. Three new species are named from Thailand including Paraisaria orthopterorum, P. phuwiangensis, and P. yodhathaii. New species combinations are made for Ophiocordyceps amazonica, O. blattarioides, O. coenomyiae, O. gracilioides, O. gracilis, O. heteropoda, O. paramyrmicarum (= Paraisaria myrmicarum), and O. tettigonia.
Similar content being viewed by others
References
Araújo JPM, Evans HC, Kepler R, Hughes DP (2018) Zombie-ant fungi across continents: 15 new species and new combinations within Ophiocordyceps. I. Myrmecophilous hirsutelloid species. Stud Mycol 90:119–160. https://doi.org/10.1016/j.simyco.2017.12.002
Ban S, Sakane T, Toyama K, Nakagiri A (2009) Teleomorph–anamorph relationships and reclassification of Cordyceps cuboidea and its allied species. Mycoscience 50:261–272. https://doi.org/10.1007/S10267-008-0480-Y
Ban S, Sakane T, Nakagiri A (2015) Three new species of Ophiocordyceps and overview of anamorph types in the genus and the family Ophiocordycipitaceae. Mycol Prog 14:1017–1028. https://doi.org/10.1007/s11557-014-1017-8
Castlebury LA, Rossman AY, Sung GH, Hyten AS, Spatafora JW (2004) Multigene phylogeny reveals new lineage for Stachybotrys chartarum, the indoor air fungus. Mycol Res 108:864–872. https://doi.org/10.1017/S0953756204000607
Evans HC, Groden E, Bischoff JF (2010) New fungal pathogens of the red ant, Myrmica rubra, from the UK and implications for ant invasions in the USA. Fungal Biol 114:451–466. https://doi.org/10.1016/j.funbio.2010.03.007
Fan MZ, Chun-Ru L, Li ZZ (2001) Cordyceps gracilioides a new record for China. Mycosystema 20:273–274
Gorbunova LA, Kryukov Y, Zibzeev EG (2011) First records of the entomopathogenic fungus Ophiocordyceps gracilis (Ascomycota: Hypocreales) from Siberia. Euroasian Entomological Journal 92:17–18
Hall T (2004) BioEdit. Version 6.0.7. Raleigh, North Carolina: Department of Microbiology, North Carolina State University. [cited 2013 Sep 24]. Available from: http://mbio.ncsu.edu/BioEdit/bioedit.html
Hennings P (1904) Fungi amazonici II. a cl. Ernesto Ule collecti. Hedwigia 43:246–249
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Ke YH, Ju YM (2015) Two rare ophiocordycipitaceous fungi newly recorded in Taiwan. Bot Stud 56:30. https://doi.org/10.1186/s40529-015-0110-x
Kepler RM, Ban S, Nakagiri A, Bischoff J, Hywel-Jones N, Owensby CA, Spatafora JW (2013) The phylogenetic placement of hypocrealean insect pathogens in the genus Polycephalomyces: an application of one fungus one name. Fungal Biol 117:611–622. https://doi.org/10.1016/j.funbio.2013.06.002
Khonsanit A, Luangsa-ard JJ, Thanakitpipattana D, Kobmoo N, Piasai O (2018) Cryptic species within Ophiocordyceps myrmecophila complex on formicine ants from Thailand. Mycol Prog 18:147–161. https://doi.org/10.1007/s11557-018-1412-7
Kobayasi Y (1941) The genus Cordyceps and its allies. Sci. Rep. Tokyo Bunrika Daigaku. Sec B 84:53–260
Kobayasi Y (1981) Revision of the genus Cordyceps and its allies 2. Bull Natl Sci Mus, Tokyo Sec B 7:123–129
Kobayasi Y (1982) Keys to the taxa of the genera Cordyceps and Torrubiella. Trans Mycol Soc Japan 23:329–364
Kobayasi Y, Shimizu D (1960) Monographic studies of Cordyceps 1. Group parasitic on Elaphomyces. Bull Natl Sci Mus, Tokyo 5:69–85
Kobmoo N, Mongkolsamrit S, Tasanathai K, Thanakitpipattana D, Luangsa-ard JJ (2012) Molecular phylogenies reveal host-specific divergence of Ophiocordyceps unilateralis sensu lato following its host ants. Mol Ecol 21:3022–3031. https://doi.org/10.1111/j.1365-294X.2012.05574.x
Kobmoo N, Mongkolsamrit S, Wutikhun T, Tasanathai K, Khonsanit A, Thanakitpipattana D, Luangsa-ard JJ (2015) New species of Ophiocordyceps unilateralis, an ubiquitous pathogen of ants from Thailand. Fungal Biol 119:44–52. https://doi.org/10.1016/j.funbio.2014.10.008
Li CR, Ming L, Fan MZ, Li ZZ (2004) Paraisaria gracilioides comb.nov., the anamorph of Cordyceps gracilioides. Mycosystema 23:165–166
Li CR, Chen MJ, Wang M, Lin YR, Fan MZ, Li ZZ (2006) Hirsutella heteropoda sp. nov. and its teleomorph, new variety of Cordyceps heteropoda. Mycosystema 25:163–168
Lebrigand K, He LD, Thakur N, Arguel MJ, Polanowska J, Henrissat B, Record E, Magdelenat G, Barbe V, Raffaele S, Barbry P, Ewbank JJ (2016) Comparative genomic analysis of Drechmeria coniospora reveals Core and specific genetic requirements for fungal Endoparasitism of nematodes. PLoS Genet 12:e1006017. https://doi.org/10.1371/journal.pgen.1006017
Luangsa-ard J, Houbraken J, van Doorn T, Hong SB, Borman AM, Hywel-Jones NL, Samson RA (2011) Purpureocillium, a new genus for the medically important Paecilomyces lilacinus. FEMS Microbiol Lett 321:141–149. https://doi.org/10.1111/j.1574-6968.2011.02322.x
Luangsa-ard J, Tasanathai K, Thanakitpipattana D, Khonsanit A, Stadler M (2018) Novel and interesting Ophiocordyceps spp. (Ophiocordycipitaceae, Hypocreales) with superficial perithecia from Thailand. Stud Mycol 89:125–142. https://doi.org/10.1016/j.simyco.2018.02.001
Mains EB (1940) Cordyceps species from British Honduras. Mycologia 32:16–22. https://doi.org/10.2307/3754313
Mains EB (1957) Species of Cordyceps parasitic on Elaphomyces. Bull Torrey Bot Club 84:243–251. https://doi.org/10.2307/2482671
Mains EB (1958) North American entomogenous species of Cordyceps. Mycologia 50:169–222. https://doi.org/10.2307/3756193
Mains EB (1959) Cordyceps species. Bull Torrey Bot Club 86:46–58. https://doi.org/10.2307/2482660
Matočec N, Kušan I, Ozimec R (2014) The genus Polycephalomyces (Hypocreales) in the frame of monitoring Veternica cave (Croatia) with a new segregate genus Perennicordyceps. Ascomycete.org 6:125–133
Mongkolsamrit S, Luangsa-ard JJ, Spatafora JW, Sung GH, Hywel-Jones NL (2009) A combined ITS rDNA and beta-tubulin phylogeny of Thai species of Hypocrella with nonfragmenting ascospores. Mycol Res 113:684–699. https://doi.org/10.1016/j.mycres.2009.02.004
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Uppsala University, Uppsala, Sweden, Evolutionary Biology Centre
Palfner G, Valenzuela-Muñoz V, Gallardo-Escarate C, Parra LE, Becerra J, Silva M (2012) Cordyceps cuncunae (Ascomycota, Hypocreales), a new pleoanamorphic species from temperate rainforest in southern Chile. Mycol Prog 11:733–739. https://doi.org/10.1007/s11557-011-0784-8
Petch T (1931) Notes on entomogenous fungi. Trans Br Mycol Soc 16:55–75. https://doi.org/10.1016/S0007-1536(31)80006-3
Petch T (1937) Notes on entomogenous fungi. Trans Br Mycol Soc 21:34–67. https://doi.org/10.1016/S0007-1536(37)80005-4
Petch T (1938) British Hypocreales. Trans Br Mycol Soc 21:243–301. https://doi.org/10.1016/S0007-1536(38)80026-7
Quandt CA, Kepler RM, Gams W, Araújo JP, Ban S, Evans HC, Hughes D, Humber R, Hywel-Jones N, Li Z, Luangsa-ard JJ, Rehner SA, Sanjuan T, Sato H, Shrestha B, Sung GH, Yao YJ, Zare R, Spatafora JW (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
Quandt CA, Kohler A, Hesse CN, Sharpton TJ, Martin F, Spatafora JW (2015) Metagenome sequence of Elaphomyces granulatus from sporocarp tissue reveals Ascomycota ectomycorrhizal fingerprints of genome expansion and a Proteobacteria-rich microbiome. Environ Microbiol 17:2952–2968. https://doi.org/10.1111/1462-2920.12840
Rehner SA (2001) Primers for elongation factor 1-alpha (EF1-alpha). Available from: http://ocid.nacse.org/research/deephyphae/EF1primer.pdf
Rehner SA, Samuels GJ (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycol Res 98:625–634. https://doi.org/10.1016/S0953-7562(09)80409-7
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Samson RA, Brady BL (1983) Paraisaria, a new genus for Isaria dubia, the anamorph of Cordyceps gracilis. Trans Br Mycol Soc 81:285–290. https://doi.org/10.1016/S0007-1536(83)80081-3
Sanjuan TI, Franco-Molano AE, Kepler RM, Spatafora JW, Tabima J, Vasco-Palacios AM, Restrepo S (2015) Five new species of entomopathogenic fungi from the Amazon and evolution of neotropical Ophiocordyceps. Fungal Biol 119:901–916. https://doi.org/10.1016/j.funbio.2015.06.010
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109:6241–6246. https://doi.org/10.1073/pnas.1117018109
Shrestha B, Tanaka E, Hyun MW, Han JG, Kim CS, Jo JW, Han SK, Oh J, Sung GH (2016) Coleopteran and lepidopteran hosts of the entomopathogenic genus Cordyceps sensu lato. J Mycol 7648219. https://doi.org/10.1155/2016/7648219
Simmons DR, Kepler RM, Rehner SA, Groden E (2015) 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
Spatafora JW, Sung GH, Sung JM, Hywel-Jones NL, White JF (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol Ecol 16:1701–1711. https://doi.org/10.1111/j.1365-294X.2007.03225.x
Spatafora JW, Quandt CA, Kepler RM, Sung GH, Shrestha B, Hywel-Jones NL, Luangsa-ard JJ (2015) New 1F1N species combinations in Ophiocordycipitaceae (Hypocreales). IMA Fungus 6:357–362. https://doi.org/10.5598/imafungus.2015.06.02.07
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Sung GH, Hywel-Jones NL, Sung JM, Luangsa-ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57:5–59. https://doi.org/10.3114/sim.2007.57.01
Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sunderland, Massachusetts: Sinauer associates
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
Tzean SS, Hsieh LS, Wu WJ (1997) Atlas of entomopathogenic fungi from Taiwan. Council of Agriculture, Executive Yuan, Taiwan p 214
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4239–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (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. Stud Mycol 92:135–154. https://doi.org/10.1016/j.simyco.2018.05.001
Wang YB, Yu H, Dai YD, Chen ZH, Zeng WB, Yuan F, Liang ZQ (2015) Polycephalomyces yunnanensis (Hypocreales), a new species of Polycephalomyces parasitizing Ophiocordyceps nutans and stink bugs (hemipteran adults). Phytotaxa 208:34–44. https://doi.org/10.11646/phytotaxa.208.1.3
Wang YB, Nguyen TT, Dai YD, Yu H, Zeng WB, Wu CK (2018) Molecular phylogeny and morphology of Ophiocordyceps unituberculata sp. nov. (Ophiocordycipitaceae), a pathogen of caterpillars (Noctuidae, Lepidoptera) from Yunnan, China. Mycol Prog 17:745–753. https://doi.org/10.1007/s11557-017-1370-5
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, California, pp 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Wen TC, Xiao YP, Zha LS, Hyde KD, Kang JC (2016) Multigene phylogeny and morphology reveal a new species, Ophiocordyceps tettigonia, from Guizhou Province, China. Phytotaxa 280:141–151. https://doi.org/10.11646/phytotaxa.280.2.4
Xiao YP, Wen TC, Hongsanan S, Jeewon R, Luangsa-ard JJ, Brooks S, Wanasinghe DN, Long FY, Hyde KD (2018) Multigene phylogenetics of Polycephalomyces (Ophiocordycipitaceae, Hypocreales), with two new species from Thailand. Sci Rep 8:18087. https://doi.org/10.1038/s41598-018-36792-4
Xiao YP, Hongsanan S, Hyde KD, Brooks S, Xie N, Long FY, Wen TC (2019) Two new entomopathogenic species of Ophiocordyceps in Thailand. MycoKeys 47:53–74. https://doi.org/10.3897/mycokeys.47.29898
Acknowledgments
We would like to thank BIOTEC as well as CPMO for their support of the program Biodiversity studies of entomopathogenic fungi in Thailand. We also thank Mr. Artit Khonsanit for photos on the natural samples. We are grateful Mr. Samret Phusaensri (Head of Phu Wiang National Park), Mr. Kosit Nilrat (Head of Mu Ko Chang National Park), Mr. Sangaon Veeraping (Village headman of Banphao Thai community forest, Phitsanulok Province), and Mr. Witthaya Sangsawang for their cooperation and support of our research project. Thanks to Dr. Sasitorn Hasin and Mr. Itsarapong Voraphab for insect host identification. Also, we would like to thank Dr. Philip James Shaw for thoughtful editing of the manuscript. We are grateful to the two anonymous reviewers and editors whose suggestions and comments helped improve the manuscript.
Funding
This study was supported by Cluster and Program Management Office, NSTDA (Grant no. P15-51452) and Platform Technology Management Section, BIOTEC (Grant no. P19-50231).
Author information
Authors and Affiliations
Corresponding author
Additional information
Section Editor: Marc Stadler
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 2647 kb)
Rights and permissions
About this article
Cite this article
Mongkolsamrit, S., Noisripoom, W., Arnamnart, N. et al. Resurrection of Paraisaria in the Ophiocordycipitaceae with three new species from Thailand. Mycol Progress 18, 1213–1230 (2019). https://doi.org/10.1007/s11557-019-01518-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11557-019-01518-x