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Clavicipitaceous entomopathogens: new species in Metarhizium and a new genus Nigelia

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In several surveys in the tropical forests in Thailand, specimens that looked morphologically similar to Metarhizium martiale and Cordyceps variegata, as well as other Metarhizium species were collected and cultured in vitro. A combined phylogeny of several genes including the small (18S) and large (28S) subunits of the ribosomal DNA, elongation factor 1-α (TEF), RNA polymerase II subunits 1 and 2 (RPB1, RPB2) genes has shown these to be new taxa in the Clavicipitaceae. Nigelia is described as a new genus closely related to Metarhizium, to the scale insect pathogens Aschersonia (Hypocrella), Samuelsia and Moelleriella, and to plant pathogens in Claviceps and Balansia, and other relatives. Nigelia comprises M. martiale and a new species Nigelia aurantiaca, which has been found infecting lepidopteran larvae and which produces pseudoimmersed, obliquely arranged, obpyriform perithecia with curved or bent ostioles and with whole (non-separating) cylindric ascospores. Metarhizium chaiyaphumense, M. kalasinense, M. prachinense, M. samlanense, and M. takense are described as new species of Metarhizium. Metarhizium martiale is transferred to Nigelia, and Paecilomyces reniformis is transferred to Metarhizium.

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  • Bischoff JF, Rehner SA, Humber RA (2006) Metarhizium frigidum sp. nov.: a cryptic species of M. anisopliae and a member of the M. flavoviride complex. Mycologia 98(5):737–745. doi:10.3852/mycologia.98.5.737

    Article  CAS  PubMed  Google Scholar 

  • Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101(4):512–530. doi:10.3852/07-202

    Article  CAS  PubMed  Google Scholar 

  • Castlebury LA, Rossman AY, Sung G-H, Hyten AS, Spatafora JW (2004) Multigene phylogeny reveals new lineage for Stachybotrys chartarum, the indoor air fungus. Mycol Res 108:864–872. doi:10.1017/S0953756204000607

    Article  CAS  PubMed  Google Scholar 

  • Chaverri P, Bischoff JF, Evans HC, Hodge KT (2005) Regiocrella, a new entomopathogenic genus with a pycnidial anamorph and its phylogenetic placement in the Clavicipitaceae. Mycologia 97:1225–1237. doi:10.3852/mycologia.97.6.1225

    Article  PubMed  Google Scholar 

  • Dettman JR, Habinski FM, Taylor JW (2001) Ascospore morphology is a poor predictor of the phylogenetic relationships of Neurospora and Gelasinospora. Fungal Genet Biol 34:49–61. doi:10.1006/fgbi.2001.1289

    Article  CAS  PubMed  Google Scholar 

  • Driver F, Milner RJ, Trueman JWH (2000) A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data. Mycol Res 104:134–150. doi:10.1017/S0953756299001756

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gams W, Jaklitsch W, Agerer R, Aguirre-Hudson B, Andersen B, Aptroot A, Barreto RW, Beck A, Benkert D, Braun U et al (2011) A critical response to the ‘Amsterdam Declaration’. Mycotaxon 116:501–512. doi:10.5248/116.501

    Article  Google Scholar 

  • Gams W, Baral HO, Jaklitsch WM, Kirschner R, Stadler M (2012a) Clarifications needed concerning the new Article 59 dealing with pleomorphic fungi. IMA Fungus 3:175–177. doi:10.5598/imafungus.2012.03.02.09

    Article  PubMed  PubMed Central  Google Scholar 

  • Gams W, Humber RA, Jaklitsch W, Kirschner R, Stadler M (2012b) Minimizing the chaos following the loss of Article 59: suggestions for a discussion. Mycotaxon 119:495–507. doi:10.5248/119.495

    Article  Google Scholar 

  • Hall T (2004) BioEdit, version 6.0.7. Department of Microbiology, North Carolina State University.

  • Hawksworth DL (2011) A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. IMA Fungus 2:155–162. doi:10.5598/imafungus.2011.02.02.06

    Article  PubMed  PubMed Central  Google Scholar 

  • Hennig W (1950) Grundzüge einer Theorie der phylogenetischen Systematik. Deutscher Zentralverlag, Berlin

    Google Scholar 

  • Johnson D, Sung G-H, Hywel-Jones NL, Luangsa-Ard JJ, Bischoff JF, Kepler RM, Spatafora JW (2009) Systematics and evolution of the genus Torrubiella (Hypocreales, Ascomycota). Mycol Res 113:279–289. doi:10.1016/j.mycres.2008.09.008

    Article  CAS  PubMed  Google Scholar 

  • Kepler RM, Sung G-H, Ban S, Nakagiri A, Chen M-J, Huang B, Li Z, Spatafora JW (2012) New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia 104:182–197. doi:10.3852/11-070

    Article  CAS  PubMed  Google Scholar 

  • Kepler RM, Ban S, Nakagiri A, Bischoff J, Hywel-Jones NL, 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. doi:10.1016/j.funbio.2013.06.002

    Article  PubMed  Google Scholar 

  • Kepler RM, Humber RA, Bischoff JF, Rehner SA (2014) Clarification of generic and species boundaries for Metarhizium and related fungi through multigene phylogenetics. Mycologia 106(4):811–829. doi:10.3852/13-319

    Article  PubMed  Google Scholar 

  • Kobayasi Y (1941) The genus Cordyceps and its allies. Sci Rep Tokyo Bun Daigaku 5(84):53–260

    Google Scholar 

  • Kobayasi Y, Shimizu D (1963). Monographic studies of Cordyceps 2. Group parasitic on Cicadae. Bull Natl Sci Mus Tokyo 6:286–314

  • Kornerup A, Wanscher JH (1963) Methuen Handbook of colour. Methue, London

  • Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. Mol Evol 20(1):86–93

    Article  CAS  Google Scholar 

  • Li CR, Huang B, Fan MZ, Lin YG, Li ZZ (2010) Metacordyceps guniujiangensis and its Metarhizium anamorph: a new pathogen on cicada nymphs. Mycotaxon 111:221–231

  • Li Z, Li C, Huang B, Fan M (2001) Discovery and demonstration of the teleomorph of Beauveria bassiana (Bals.) Vuill., an important entomogenous fungus. Chin Sci Bull 46:751–753. doi:10.1007/BF03187215

    Article  Google Scholar 

  • Liang ZQ, Liu AY (1991) A new species of the genus Cordyceps and its Metarhizium anamorph. Acta Mycol Sin 10:257–262

  • Liu M, Rombach MC, Humber RA, Hodge KT (2005) What’s in a name? Aschersonia insperata: a new pleoanamorphic fungus with characteristics of Aschersonia and Hirsutella. Mycologia 97:246–253. doi:10.3852/mycologia.97.1.246

    PubMed  Google Scholar 

  • Liu ZY,Liang ZQ, Whalley AJS, Yao Y-J, Liu AY (2001) Cordyceps brittlebankisoides, a new pathogen of grubs and its anamorph, Metarhizium anisopliae var. majus. J Invert Pathol 78:178–182

  • Luangsa-ard JJ, Hywel-Jones NL, Samson RA (2004) The polyphyletic nature of Paecilomyces sensu lato based on 18S-generated rRNA phylogeny. Mycologia 96:773–780

    Article  CAS  PubMed  Google Scholar 

  • Luangsa-ard JJ, Hywel-Jones NL, Manoch L, Samson RA (2005) On the relationships of Paecilomyces sect. Isarioidea species. Mycol Res 109:581–589

    Article  CAS  PubMed  Google Scholar 

  • Lumbsch HT, Huhndorf SM (2007) Whatever happened to the pyrenomycetes and the loculoascomycetes? Mycol Res 111:1064–1074. doi:10.1016/j.mycres.2007.04.004

    Article  PubMed  Google Scholar 

  • Mains EB (1958) North American entomogenous species of Cordyceps. Mycologia 50:169–222. doi:10.2307/3756193

    Article  Google Scholar 

  • Miller AN, Huhndorf SM (2005) Multi-gene phylogenies indicate ascomal wall morphology is a better predictor of phylogenetic relationships than ascospore morphology in the Sordariales (Ascomycota, Fungi). Mol Phylogenet Evol 35:60–75. doi:10.1016/j.ympev.2005.01.007

    Article  CAS  PubMed  Google Scholar 

  • Moureau J (1949) Cordyceps Du Congo Belge. Mem. Inst. Royal Colonial Belge

  • Nylander JAA (2004) MrModeltest 2.2: program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • Quandt CA, Kepler RM, Gams W, Araújo JPM, Ban S, Evans HC, Hughes D, Humber R, Hywel-Jones NL, Li Z, Luangsa-ard JJ, Rehner SA, Sanjuan T, Sato H, Shrestha B, Sung G-H, Yao Y-J, Zare R, Spatafora JW (2014) Phylogenetic-based nomenclatural proposals for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium. IMA Fungus 5(1):121–134. doi:10.5598/imafungus.2014.05.01.12

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Samson RA (1974) Paecilomyces and some allied hyphomycetes. Stud Mycol 6:1–119

    Google Scholar 

  • Smithe FB (1975) Naturalist’s Color Guide. The American Museum of Natural History, New York

  • Spatafora JW, Sung G-H, Sung J-M, Hywel-Jones NL, Jr White JF (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol Ecol 16:1701–1711. doi:10.1111/j.1365-294X.2007.03225.x

    Article  CAS  PubMed  Google Scholar 

  • Spatafora JW, Quandt CA, Kepler RM, Sung G-H, Shrestha B, Hywel-Jones NL, Luangsa-ard JJ (2015) New 1F1N species combinations in Ophiocordycipitaceae (Hypocreales). IMA Fungus 6(2):357–362. doi:10.5598/imafungus.2015.06.02.07

    Article  PubMed  PubMed Central  Google Scholar 

  • Spegazzini C (1889) Fungi Puiggariani. Pugillus 1. Bol Acad Nac Cien Córdoba 11(4):381–622

    Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. doi:10.1093/bioinformatics/btu033

  • Sung G-H, Sung J-M, Hywel-Jones NL, Spatafora JW (2007a) A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): Identification of localized incongruence using a combinational bootstrap approach. Mol Phylogenet Evol 44:1204–1223. doi:10.1016/j.ympev.2007.03.011

    Article  CAS  PubMed  Google Scholar 

  • Sung G-H, Hywel-Jones NL, Sung J-M, Luangsa-ard JJ, Shrestha B, Spatafora JW (2007b) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57:5–66. doi:10.3114/sim.2007.57.01

    Article  PubMed  PubMed Central  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (* and other methods) Version 4.0b10. Sinauer, Sunderland

  • Tzean SS, Hsieh LS, Chen JL, Wu WJ (1993) Nomuraea cylindrospora comb. nov. Mycologia 85:514–519

  • Vellinga EC, Kuyper TW, Ammirati J, Dejardin DE, Halling RE, Justo A, Læssøe T, Lebel T, Lodge DJ, Matheny PB, Methven AS, Moreau P-A, Mueller GM, Noordeloos ME, Nuytinck J, Ovrebo CL, Verbeken A (2015) Six simple guidelines for introducing new genera of fungi. IMA Fungus 6:65–68

    Google Scholar 

  • 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, San Diego, pp 315–322

    Google Scholar 

  • Wiens JJ (1998) Combining data sets with different phylogenetic histories. Syst Biol 47:568–581. doi:10.1080/106351598260581

    Article  CAS  PubMed  Google Scholar 

  • Zang M, Liu DQ, Hu RY (1982). Notes concerning the subdivisions of Cordyceps and a new species from China. Acta Bot Yunnan 4:173–176

  • Zhang WM, Li TH, Chen YQ, Qu LH (2004) Cordyceps campsosterna, a new pathogen of Campsosternus auratus. Fungal Divers 17:239–242

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The authors would like to thank Drs Lily Eurwilaichitr, Kanyawim Kirtikara (BIOTEC), Prof. Morakot Tanticharoen, and Khun Rungsima Tantalakha for the support of the project. This project was supported by Cluster and Program Management Office grant number P15-51452. Some of the collections were made by Dr Nigel Hywel-Jones, who is thanked for his early contributions to this project. We wish to thank Mr. Rungpet Ridkaew for his earlier contributions to this study. We also wish to thank Prof. Drion Boucias, for sending the Paecilomyces reniformis strains to study. We thank the Thailand Department of National Parks for the permission to collect fungi in the national parks. We are grateful to the anonymous reviewers who made valuable comments and suggestions to improve the manuscript.

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Correspondence to J. Jennifer Luangsa-ard.

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Section Editor: Hans-Josef Schroers

This article is part of the “Special Issue in honour of the 70th birthday of Dr. Eric McKenzie”

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Luangsa-ard, J.J., Mongkolsamrit, S., Thanakitpipattana, D. et al. Clavicipitaceous entomopathogens: new species in Metarhizium and a new genus Nigelia . Mycol Progress 16, 369–391 (2017).

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