Abstract
Gibellula is an exclusively spider-pathogen genus, with most species immediately recognized by their distinctive conidial state, but also including the teleomorphic states of these fungi that were previously included in the rejected genus Torrubiella. Two sexual specimens and an asexual morph specimen were collected from Anhui Province, China, and were recognized as the same species based on molecular evidence. Its asexual morph differs from Gibellula pulchra, to which it is morphologically similar, in having shorter verrucose conidiophores with slightly smaller metulae, phialides and conidia. Its sexual morph is characterized by producing superficial and elongate ellipsoid small perithecia with short asci on a cream-yellow mycelial mat covering the host. Multi-locus (SSU, LSU, TEF, and RPB1) phylogenetic analyses showed that the specimens belong to a strongly supported subclade, and formed a sister subclade with G. pulchra and Gibellula sp. A combination of morphological characteristics and its phylogenetic placement confirmed that these unique specimens are a new species, which is described as Gibellula flava.
References
<p>Bischoff, J.F. & White, Jr.J.F. (2004) <em>Torrubiella piperis</em> <em>sp. nov.</em> (Clavicipitaceae, Hypocreales), a new teleomorph of the <em>Lecanicillium</em> complex. <em>Studies in Mycology</em> 50: 89–94.</p>
<p>Bischoff, J.F., Rehner, S.A. & Humber, R.A. (2009) A multilocus phylogeny of the <em>Metarhizium anisopliae</em> lineage. <em>Mycologia </em>101: 512–530. https://doi.org/10.3852/07-202</p>
<p>Castlebury, L.A., Rossman, A.Y., Sung, G.H., Hyten, A.S. & Spatafora, J.W. (2004) Multigene phylogeny reveals new lineage for <em>Stachybotrys chartarum</em>, the indoor air fungus. <em>Mycological Research </em>108: 864–872. https://doi.org/10.1017/s0953756204000607</p>
<p>Chen, W.H., Han, Y.F., Liang, J.D., Tian, W.Y. & Liang, Z.Q. (2020) Morphological and phylogenetic characterisations reveal three new species of <em>Samsoniella</em> (Cordycipitaceae, Hypocreales) from Guizhou, China. <em>MycoKeys </em>74: 1–15. https://doi.org/10.3897/mycokeys.74.56655</p>
<p>Chirivi, J., Danies, G., Sierra, R., Schauer, N., Trenkamp, S., Restrepo, S. & Sanjuan, T. (2017) Metabolomic profile and nucleoside composition of <em>Cordyceps nidus</em> <em>sp. nov.</em> (Cordycipitaceae): a new source of active compounds. <em>PLoS One </em>12: e0179428. https://doi.org/10.1371/journal.pone.0179428</p>
<p>Evans, H.C. (2013) Fungal pathogens of spiders. <em>In:</em> Nentwig, W. (Ed.) <em>Spider ecophysiology. </em>Springer, Berlin, Heidelberg, pp. 107–121. https://doi.org/10.1007/978-3-642-33989-99</p>
<p>Gardes, M. & Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes –application to the identification of mycorrhizae and rusts. <em>Molecular Ecology </em>2: 113–118. https://doi.org/10.1111/j.1365-294x.1993.tb00005.x</p>
<p>Hall, T. (2011) BioEdit: an important software for molecular biology. <em>GERF Bulletin of Biosciences </em>2: 60–61.</p>
<p>Helaly, S.E., Kuephadungphan, W., Phainuphong, P., Ibrahim, M.A.A., Tasanathai, K., Mongkolsamrit, S., Luangsa-ard, J.J., Phongpaichit, S., Rukachaisirikul, V. & Stadler, M. (2019) Pigmentosins from <em>Gibellula</em> sp. as antibiofilm agents and a new glycosylated asperfuran from <em>Cordyceps javanica</em>. <em>Beilstein Journal of Organic Chemistry </em>15: 2968–2981. https://doi.org/10.3762/bjoc.15.293</p>
<p>Jaklitsch, W.M. & Voglmayr, H. (2015) Biodiversity of <em>Trichoderma</em> (Hypocreaceae) in Southern Europe and Macaronesia. <em>Studies in Mycology </em>80: 1–87. https://doi.org/10.1016/j.simyco.2014.11.001</p>
<p>Johnson, T. (1968) Host specialization as a taxonomic criterion. <em>In</em>: Ainsworth, G.C. & Sussman, A.S. (Eds.) <em>The fungi advanced treatise. Volume III. The fungal population</em>. Academic Press, New York, pp. 543–554. https://doi.org/10.1016/B978-1-4832-2744-3.50027-4</p>
<p>Johnson, D., Sung, G.H., Hywel-Jones, N.L., Luangsa-ard, J.J., Bischoff, J.F., Kepler, R.M. & Spatafora, J.W. (2009) Systematics and evolution of the genus <em>Torrubiella</em> (Hypocreales, Ascomycota). <em>Mycological Research </em>113: 279–289. https://doi.org/10.1016/j.mycres.2008.09.008</p>
<p>Kepler, R.M., Luangsa-ard, J.J., Hywel-Jones, N.L., Quandt, C.A., Sung, G.H., Rehner, S.A., Aime, M.C., Henkel, T.W., Sanjuan, T., Zare, R., Chen, M., Li, Z., Rossman, A.Y., Spatafora, J.W. & Shrestha, B. (2017) A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). <em>IMA Fungus </em>8: 335–353. https://doi.org/10.5598/imafungus.2017.08.02.08</p>
<p>Kuephadungphan, W., Macabeo, A.P.G., Luangsa-ard, J.J., Tasanathai, K., Thanakitpipattana, D., Phongpaichit, S., Yuyama, K. & Stadler, M. (2019) Studies on the biologically active secondary metabolites of the new spider parasitic fungus <em>Gibellula gamsii</em>. <em>Mycological Progress </em>18: 135–146. https://doi.org/10.1007/s11557-018-1431-4</p>
<p>Kuephadungphan, W., Tasanathai, K., Petcharad, B., Khonsanit, A., Stadler, M. & Luangsa-ard, J.J. (2020) Phylogeny- and morphology-based recognition of new species in the spider-parasitic genus <em>Gibellula</em> (Hypocreales, Cordycipitaceae) from Thailand. <em>MycoKeys </em>72: 17–42. https://doi.org/10.3897/mycokeys.72.55088</p>
<p>Mains, E.B. (1950) The genus <em>Gibellula </em>on spiders in North America. <em>Mycologia</em> 42: 306–321. https://doi.org/10.1080/00275514.1950.12017836</p>
<p>Mongkolsamrit, S., Noisripoom, W., Thanakitpipattana, D., Wutikhun, T., Spatafora, J.W. & Luangsa-ard, J. (2018) Disentangling cryptic species with<em> Isaria</em>-like morphs in Cordycipitaceae. <em>Mycologia </em>110: 230–257. https://doi.org/10.1080/00275514.2018.1446651</p>
<p>Mongkolsamrit, S., Khonsanit, A., Thanakitpipattana, D., Tasanathai, K., Noisripoom, W., Lamlertthon, S., Himaman, W., Houbraken, J., Samson, R.A. & Luangsa-ard, J. (2020) Revisiting <em>Metarhizium</em> and the description of new species from Thailand. <em>Studies in Mycology </em>95: 171–251. https://doi.org/10.1016/j.simyco.2020.04.001</p>
<p>Petch, T. (1923) Studies in entomogenous fungi. III. <em>Torrubiella</em>. <em>Transactions of the British Mycological Society </em>9: 108–128. https://doi.org/10.1016/S0007-1536(23)80018-3</p>
<p>Rehner, S.A. & Buckley, E. (2005) A <em>Beauveria</em> phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to <em>Cordyceps</em> teleomorphs. <em>Mycologia </em>97 (1): 84–98. https://doi.org/10.1080/15572536.2006.11832842</p>
<p>Rehner, S.A., Minnis, A.M., Sung, G.H., Luangsa-ard, J.J., Devotto, L. & Humber, R.A. (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus <em>Beauveria</em>. <em>Mycologia </em>103: 1055–1073. https://doi.org/10.3852/10-302</p>
<p>Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. <em>Bioinformatics </em>19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180</p>
<p>Samson, R.A. & Evans, H.C. (1973) Notes on entomogenous fungi from Ghana I. The genera <em>Gibellula </em>and <em>Pseudogibellula</em>. <em>Acta Botanica Neerlandica </em>22: 522–528. https://doi.org/10.1111/j.1438-8677.1973.tb00873.x</p>
<p>Sanjuan, T., Tabima, J., Restrepo, S., Læssøe, T., Spatafora, J.W. & Franco-Molano, A.E. (2014) Entomopathogens of Amazonian stick insects and locusts are members of the <em>Beauveria</em> species complex (<em>Cordyceps </em>sensu stricto). <em>Mycologia </em>106: 260–275. https://doi.org/10.3852/13-020</p>
<p>Shrestha, B., Kubátová, A., Tanaka, E., Oh, J., Yoon, D.H., Sung, J.M. & Sung, G.H. (2019) Spider-pathogenic fungi within Hypocreales (Ascomycota): their current nomenclature, diversity, and distribution. <em>Mycological Progress </em>18: 983–1003. https://doi.org/10.1007/s11557-019-01512-3</p>
<p>Spatafora, J.W., Volkmann-Kohlmeyer, B. & Kohlmeyer, J. (1998) Independent terrestrial origins of the Halosphaeriales (Marine Ascomycota). <em>American Journal of Botany </em>85: 1569–1580. https://doi.org/10.2307/2446483</p>
<p>Spatafora, J.W., Sung, G.H., Sung, J.M., Hywel-Jones, N.L. & White, J.F. (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. <em>Molecular Ecology </em>16: 1701–1711. https://doi.org/10.1111/j.1365-294X.2007.03225.x</p>
<p>Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. <em>Bioinformatics </em>22: 2688–2690. https://doi.org/10.1093/bioinformatics/btl446</p>
<p>White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. <em>In</em>: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.) <em>PCR protocols: a guide to methods and applications</em>. Academic Press, New York, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1</p>
<p>Bischoff, J.F., Rehner, S.A. & Humber, R.A. (2009) A multilocus phylogeny of the <em>Metarhizium anisopliae</em> lineage. <em>Mycologia </em>101: 512–530. https://doi.org/10.3852/07-202</p>
<p>Castlebury, L.A., Rossman, A.Y., Sung, G.H., Hyten, A.S. & Spatafora, J.W. (2004) Multigene phylogeny reveals new lineage for <em>Stachybotrys chartarum</em>, the indoor air fungus. <em>Mycological Research </em>108: 864–872. https://doi.org/10.1017/s0953756204000607</p>
<p>Chen, W.H., Han, Y.F., Liang, J.D., Tian, W.Y. & Liang, Z.Q. (2020) Morphological and phylogenetic characterisations reveal three new species of <em>Samsoniella</em> (Cordycipitaceae, Hypocreales) from Guizhou, China. <em>MycoKeys </em>74: 1–15. https://doi.org/10.3897/mycokeys.74.56655</p>
<p>Chirivi, J., Danies, G., Sierra, R., Schauer, N., Trenkamp, S., Restrepo, S. & Sanjuan, T. (2017) Metabolomic profile and nucleoside composition of <em>Cordyceps nidus</em> <em>sp. nov.</em> (Cordycipitaceae): a new source of active compounds. <em>PLoS One </em>12: e0179428. https://doi.org/10.1371/journal.pone.0179428</p>
<p>Evans, H.C. (2013) Fungal pathogens of spiders. <em>In:</em> Nentwig, W. (Ed.) <em>Spider ecophysiology. </em>Springer, Berlin, Heidelberg, pp. 107–121. https://doi.org/10.1007/978-3-642-33989-99</p>
<p>Gardes, M. & Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes –application to the identification of mycorrhizae and rusts. <em>Molecular Ecology </em>2: 113–118. https://doi.org/10.1111/j.1365-294x.1993.tb00005.x</p>
<p>Hall, T. (2011) BioEdit: an important software for molecular biology. <em>GERF Bulletin of Biosciences </em>2: 60–61.</p>
<p>Helaly, S.E., Kuephadungphan, W., Phainuphong, P., Ibrahim, M.A.A., Tasanathai, K., Mongkolsamrit, S., Luangsa-ard, J.J., Phongpaichit, S., Rukachaisirikul, V. & Stadler, M. (2019) Pigmentosins from <em>Gibellula</em> sp. as antibiofilm agents and a new glycosylated asperfuran from <em>Cordyceps javanica</em>. <em>Beilstein Journal of Organic Chemistry </em>15: 2968–2981. https://doi.org/10.3762/bjoc.15.293</p>
<p>Jaklitsch, W.M. & Voglmayr, H. (2015) Biodiversity of <em>Trichoderma</em> (Hypocreaceae) in Southern Europe and Macaronesia. <em>Studies in Mycology </em>80: 1–87. https://doi.org/10.1016/j.simyco.2014.11.001</p>
<p>Johnson, T. (1968) Host specialization as a taxonomic criterion. <em>In</em>: Ainsworth, G.C. & Sussman, A.S. (Eds.) <em>The fungi advanced treatise. Volume III. The fungal population</em>. Academic Press, New York, pp. 543–554. https://doi.org/10.1016/B978-1-4832-2744-3.50027-4</p>
<p>Johnson, D., Sung, G.H., Hywel-Jones, N.L., Luangsa-ard, J.J., Bischoff, J.F., Kepler, R.M. & Spatafora, J.W. (2009) Systematics and evolution of the genus <em>Torrubiella</em> (Hypocreales, Ascomycota). <em>Mycological Research </em>113: 279–289. https://doi.org/10.1016/j.mycres.2008.09.008</p>
<p>Kepler, R.M., Luangsa-ard, J.J., Hywel-Jones, N.L., Quandt, C.A., Sung, G.H., Rehner, S.A., Aime, M.C., Henkel, T.W., Sanjuan, T., Zare, R., Chen, M., Li, Z., Rossman, A.Y., Spatafora, J.W. & Shrestha, B. (2017) A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). <em>IMA Fungus </em>8: 335–353. https://doi.org/10.5598/imafungus.2017.08.02.08</p>
<p>Kuephadungphan, W., Macabeo, A.P.G., Luangsa-ard, J.J., Tasanathai, K., Thanakitpipattana, D., Phongpaichit, S., Yuyama, K. & Stadler, M. (2019) Studies on the biologically active secondary metabolites of the new spider parasitic fungus <em>Gibellula gamsii</em>. <em>Mycological Progress </em>18: 135–146. https://doi.org/10.1007/s11557-018-1431-4</p>
<p>Kuephadungphan, W., Tasanathai, K., Petcharad, B., Khonsanit, A., Stadler, M. & Luangsa-ard, J.J. (2020) Phylogeny- and morphology-based recognition of new species in the spider-parasitic genus <em>Gibellula</em> (Hypocreales, Cordycipitaceae) from Thailand. <em>MycoKeys </em>72: 17–42. https://doi.org/10.3897/mycokeys.72.55088</p>
<p>Mains, E.B. (1950) The genus <em>Gibellula </em>on spiders in North America. <em>Mycologia</em> 42: 306–321. https://doi.org/10.1080/00275514.1950.12017836</p>
<p>Mongkolsamrit, S., Noisripoom, W., Thanakitpipattana, D., Wutikhun, T., Spatafora, J.W. & Luangsa-ard, J. (2018) Disentangling cryptic species with<em> Isaria</em>-like morphs in Cordycipitaceae. <em>Mycologia </em>110: 230–257. https://doi.org/10.1080/00275514.2018.1446651</p>
<p>Mongkolsamrit, S., Khonsanit, A., Thanakitpipattana, D., Tasanathai, K., Noisripoom, W., Lamlertthon, S., Himaman, W., Houbraken, J., Samson, R.A. & Luangsa-ard, J. (2020) Revisiting <em>Metarhizium</em> and the description of new species from Thailand. <em>Studies in Mycology </em>95: 171–251. https://doi.org/10.1016/j.simyco.2020.04.001</p>
<p>Petch, T. (1923) Studies in entomogenous fungi. III. <em>Torrubiella</em>. <em>Transactions of the British Mycological Society </em>9: 108–128. https://doi.org/10.1016/S0007-1536(23)80018-3</p>
<p>Rehner, S.A. & Buckley, E. (2005) A <em>Beauveria</em> phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to <em>Cordyceps</em> teleomorphs. <em>Mycologia </em>97 (1): 84–98. https://doi.org/10.1080/15572536.2006.11832842</p>
<p>Rehner, S.A., Minnis, A.M., Sung, G.H., Luangsa-ard, J.J., Devotto, L. & Humber, R.A. (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus <em>Beauveria</em>. <em>Mycologia </em>103: 1055–1073. https://doi.org/10.3852/10-302</p>
<p>Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. <em>Bioinformatics </em>19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180</p>
<p>Samson, R.A. & Evans, H.C. (1973) Notes on entomogenous fungi from Ghana I. The genera <em>Gibellula </em>and <em>Pseudogibellula</em>. <em>Acta Botanica Neerlandica </em>22: 522–528. https://doi.org/10.1111/j.1438-8677.1973.tb00873.x</p>
<p>Sanjuan, T., Tabima, J., Restrepo, S., Læssøe, T., Spatafora, J.W. & Franco-Molano, A.E. (2014) Entomopathogens of Amazonian stick insects and locusts are members of the <em>Beauveria</em> species complex (<em>Cordyceps </em>sensu stricto). <em>Mycologia </em>106: 260–275. https://doi.org/10.3852/13-020</p>
<p>Shrestha, B., Kubátová, A., Tanaka, E., Oh, J., Yoon, D.H., Sung, J.M. & Sung, G.H. (2019) Spider-pathogenic fungi within Hypocreales (Ascomycota): their current nomenclature, diversity, and distribution. <em>Mycological Progress </em>18: 983–1003. https://doi.org/10.1007/s11557-019-01512-3</p>
<p>Spatafora, J.W., Volkmann-Kohlmeyer, B. & Kohlmeyer, J. (1998) Independent terrestrial origins of the Halosphaeriales (Marine Ascomycota). <em>American Journal of Botany </em>85: 1569–1580. https://doi.org/10.2307/2446483</p>
<p>Spatafora, J.W., Sung, G.H., Sung, J.M., Hywel-Jones, N.L. & White, J.F. (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. <em>Molecular Ecology </em>16: 1701–1711. https://doi.org/10.1111/j.1365-294X.2007.03225.x</p>
<p>Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. <em>Bioinformatics </em>22: 2688–2690. https://doi.org/10.1093/bioinformatics/btl446</p>
<p>White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. <em>In</em>: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.) <em>PCR protocols: a guide to methods and applications</em>. Academic Press, New York, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1</p>