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Issue: Vol. 644 No. 4: 17 Apr. 2024
Type: Article
Published: 2024-04-17
DOI: 10.11646/phytotaxa.644.4.1
Page range: 243-257
Abstract views: 58
PDF downloaded: 2

Microfungi associated with dead caterpillars and spiders in Xishuangbanna Tropical Botanical Garden, P.R. China

Gardening and Horticulture Department, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan 666303, P.R. China, Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing, Yunnan 655011, P.R. China, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing, Yunnan 655011, P.R. China, National Institute of Fundamental Studies (NIFS), Kandy 2000, Sri Lanka
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing, Yunnan 655011, P.R. China
Department of Botany and Microbiology, College of Sciences, King Saud University, Riyadh 11451, Saudi Arabia
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing, Yunnan 655011, P.R. China
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing, Yunnan 655011, P.R. China
Gardening and Horticulture Department, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan 666303, P.R. China
Fungi Ascomycota Curvularia geniculata entomopathogenic fungi Purpureocillium atypicola

Abstract

During an investigation of microfungi associated with insects in the tropical region of Yunnan Province, China, dead fungi infected within several caterpillars and spiders in the Xishuangbanna Tropical Botanical Garden were found. Two selected fungal strains were isolated from the surface of the cadavers and subjected to morphological and molecular identification. Phylogenetic analyses were carried out on the subsequent isolates based on multiple gene sequences (ITS, LSU, SSU, rpb1, gapdh, and tef1-α). The observations and the analyses confirmed that the fungi belong to Curvularia geniculata (associated with dead caterpillars) and Purpureocillium atypicola (associated with dead spiders). Here, we have given detailed descriptions of the species along with photo plates and phylogenetic trees showing their taxonomic placements.

References

  1. Angelo, I.C., Fernandes, É.K.K., Bahiense, T.C., Perinotto, W.M.S., Golo, P.S., Moraes, A.P.R. & Bittencourt, V.R.E.P. (2012) Virulence of Isaria sp. and Purpureocillium lilacinum to Rhipicephalus microplus tick under laboratory conditions. Parasitology Research 111: 1473–1480. https://doi.org/10.1007/s00436-012-2982-y
  2. Baldrian, P., Vetrovský, T., Lepinay, C. & Kohout, P. (2022) High-throughput sequencing view on the magnitude of global fungal diversity. Fungal Diversity 114: 539–47. https://doi.org/10.1007/s13225-021-00472-y
  3. Behie, S.W., Jones, S.J. & Bidochka, M.J. (2015) Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecology 13: 112–119. https://doi.org/10.1016/j.funeco.2014.08.001
  4. Berbee, M.L., Pirseyedi, M. & Hubbard, S. (1999) Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia 91: 964–977. https://doi.org/10.1080/00275514.1999.12061106
  5. Blackwell, M. (2011) The Fungi: 1, 2, 3… 5.1 million species?. American Journal of Botany 98: 426–438. https://doi.org/10.3732/ajb.1000298
  6. Calvillo‐Medina, R.P., Ponce‐Angulo, D.G., Raymundo, T., Müller‐Morales, C.A., Escudero‐Leyva, E., Campos Guillen, J. & Bautista‐de Lucio, V.M. (2021) Purpureocillium roseum sp. nov. A new ocular pathogen for humans and mice resistant to antifungals. Mycoses 64: 162–173. https://doi.org/10.1111/myc.13198
  7. Carter, E. & Boudreaux, C. (2004) Fatal cerebral phaeohyphomycosis due to Curvularia lunata in an immunocompetent patient. Journal of Clinical Microbiology 42: 5419–5423. https://doi.org/10.1128/JCM.42.11.5419-5423.2004
  8. Catania, M.V., Sanjuan, T.I. & Robledo, G.L. (2018) South American Cordyceps s. l. (Hypocreales, Ascomycota): first assessment of species diversity in Argentina. Nova Hedwigia 106: 261–281. https://doi.org/10.1127/nova_hedwigia/2017/0434
  9. Chen, W. & Hu, Q. (2021) Secondary metabolites of Purpureocillium lilacinum. Molecules 27: 18. https://doi.org/10.3390/molecules27010018
  10. Coyle, F.A. Goloboff, P.A. & Samson, R.A. (1990) Actinopus trapdoor spiders (Araneae, Actinopodidae) killed by the fungus, Nomuraea atypicola (Deuteromycotina). Acta Zoologica Fennica 190: 89–93.
  11. Dharpure, S.R. & Rai, M.K. (2002) New record of an entomogenous fungus Curvularia verruculosa on Leucinodes orbonalis in MP. Journal of the Indian Potato Association 29: 93
  12. Erixon, P., Svennblad, B., Britton, T. & Oxelman, B. (2003) Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Systematic Biology 52: 665–673. https://doi.org/10.1080/10635150390235485
  13. Evans, H.C. (2013) Fungal pathogens of spiders. In: Nentwig, W. (Ed.) Spider Ecophysiology. Springer, Berlin, Heidelberg, Germany, pp. 107–121.https://doi.org/10.1007/978-3-642-33989-9_9
  14. Fiorin, É.V., Brigatto, M.C.B., Jardim, P.H.A., Chang, M.R., Leal, C.R.B. & Araújo, M.A. (2021) Granulomatous tracheitis and dermatitis due to Curvularia sp. in a horse: case report. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 73: 431–437. https://doi.org/10.1590/1678-4162-12162
  15. Gine, A. & Sorribas, F.J. (2017) Effect of plant resistance and BioAct WG (Purpureocillium lilacinum strain 251) on Meloidogyne incognita in a tomato-cucumber rotation in a greenhouse. Pest Management Science 73: 880–887. https://doi.org/10.1002/ps.4357
  16. Glez-Peña, D., Gómez-Blanco, D., Reboiro-Jato, M., Fdez-Riverola, F. & Posada, D. (2010) ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Research 38: 14–18. https://doi.org/10.1093/nar/gkq321
  17. Gray, G.R. (1858) Notices of insects that are known to form the bases of fungoid parasites. British Museum, London, UK, 22 pp.
  18. Greenstone, M.H., Ignoffo, C.M. & Samson, R.A. (1987) Susceptibility of spider species to the fungus Nomuraea atypicola. The Journal of Arachnology 15: 266–268.
  19. Hall, T.A. (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98. https://doi.org/10.1021/bk-1999-0734.ch008
  20. Hotaka, D., Amnuaykanjanasin, A., Maketon, C., Siritutsoontorn, S. & Maketon, M. (2015) Efficacy of Purpureocillium lilacinum CKPL-053 in controlling Thrips palmi (Thysanoptera: Thripidae) in orchid farms in Thailand. Applied Entomology and Zoology 50: 317–329. https://doi.org/10.1007/s13355-015-0339-6
  21. Huang, Q., Zhang, L.G., Wu, Y., Reardon, R.C. & Qiang, S. (2017) The first report of leaf spot disease on Microstegium vimineum caused by Curvularia geniculata in China. Plant Disease 101: 387–387. https://doi.org/10.1094/PDIS-07-16-1074-PDN
  22. Hywel-Jones, N.L. & Sivichai, S. (1995) Cordyceps cylindrica and its association with Nomuraea atypicola in Thailand. Mycological Research 99: 809–812. https://doi.org/10.1016/S0953-7562(09)80731-4
  23. Islam, W., Adnan, M., Shabbir, A., Naveed, H., Abubakar, Y.S., Qasim, M., Tayyab, M., Noman, A., Nisar M.S., Khan, K.A. & Ali, H. (2021) Insect-fungal-interactions: A detailed review on entomopathogenic fungi pathogenicity to combat insect pests. Microbial Pathogenesis 159: 105122. https://doi.org/10.1016/j.micpath.2021.105122
  24. 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
  25. Li, C.R., Chen, A.H., Wang, M., Fan, M.Z. & Li, Z.Z. (2005) Cordyceps cylindrica and its anamorph Nomuraea atypicola. Mycosystema 24: 14–18
  26. Li, S.P., Yang, F.Q. & Tsimb, K.W.K. (2006) Quality control of Cordyceps sinensis, a valued traditional Chinese medicine. Journal of Pharmaceutical and Biomedical Analysis 41: 1571–1584. https://doi.org/10.1016/j.jpba.2006.01.046
  27. Liu, L., Cao, Y.L., Zhang, C.C., Fan, H.F., Guo, Z.Y., Yang, H.Y., Chen, M., Han, J.J., Xu, J.P., Zhang, K.Q. & Liang, L.M. (2019) An efficient gene disruption system for the nematophagous fungus Purpureocillium lavendulum. Fungal Biology 123: 274–282. https://doi.org/10.1016/j.funbio.2018.10.009
  28. Lu, X.L., Najafzadeh, M.J., Dolatabadi, S., Ran, Y.P., Gerrits van den Ende, A.H.G., Shen, Y.N., Li, C.Y., Xi, L.Y., Hao, F., Zhang, Q.Q., Li, R.Y., Hu, Z.M., Lu, G.X., Wang, J.J., Drogari-Apiranthitou, M., Klaassen, C., Meis, J.F., Hagen, F., Liu, W.D. & de Hoog, G.S. (2013) Taxonomy and epidemiology of Mucor irregularis, agent of chronic cutaneous mucormycosis. Persoonia 30: 48–56. https://doi.org/10.3767/003158513X665539
  29. Luangsa-ard, J., Houbraken, J., van Doorn, T., Hong, S.B., Borman, A.M., Hywel-Jones, N.L. & Samson, R.A. (2011) Purpureocillium, a new genus for the medically important Paecilomyces lilacinus. FEMS Microbiology Letters 321: 141–149. https://doi.org/10.1111/j.1574-6968.2011.02322.x
  30. Madrid, H., da Cunha, K.C., Gené, J., Dijksterhuis, J., Cano, J., Sutton, D.A., Guarro, J. & Crous, P.W. (2014) Novel Curvularia species from clinical specimens. Persoonia 33: 48–60. https://doi.org/10.3767/003158514X683538
  31. Manamgoda, D.S., Rossman, A.Y., Castlebury, L.A., Castlebury, L., Chukeatirote, E. & Hyde, K.D. (2015) A taxonomic and phylogenetic re-appraisal of the genus Curvularia (Pleosporaceae): human and plant pathogens. Phytotaxa 212 (3): 175–198. https://doi.org/10.11646/phytotaxa.212.3.1
  32. Manzar, N., Kashyap, A.S., Sharma, P.K. & Saxena, A.K. (2021) First report of leaf spot of maize caused by Curvularia geniculata in India. Plant Disease 105: 4155. https://doi.org/10.1094/PDIS-03-21-0637-PDN
  33. Marin-Felix, Y., Hernandez-Restrepo, M. & Crous, P.W. (2020) Multi-locus phylogeny of the genus Curvularia and description of ten new species. Mycological Progress 19: 559–588. https://doi.org/10.1007/s11557-020-01576-6
  34. Meyer, J., Loncaric, I., Richter, B. & Spergser, J. (2018) Fatal Purpureocillium lilacinum pneumonia in a green tree python. Journal of Veterinary Diagnostic Investigation 30: 305–309. https://doi.org/10.1177/1040638717750430
  35. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: IEEE (Org.) Proceedings of the 2010 Gateway Computing Environments Workshop (GCE). New Orleans, LA, USA, 14 November, pp. 1–8.https://doi.org/10.1109/GCE.2010.5676129
  36. Mpuchane, S., Taligoola, H.K. & Gashe, B.A. (1996) Fungi associated with Imbrasia belina, an edible caterpillar. Botswana Notes and Records 28: 193–197.
  37. Nemadodzi, L.E. & Prinsloo, G. (2023) A New Proposed Symbiotic Plant–Herbivore Relationship between Burkea africana Trees, Cirina forda Caterpillars and Their Associated Fungi Pleurostomophora richardsiae and Aspergillus nomius. Microorganisms 11: 1864. https://doi.org/10.3390/microorganisms11071864
  38. Niskanen, T., Lücking, R., Dahlberg, A., Gaya, E., Suz, L.M., Mikryukov, V., Liimatainen, K., Druzhinina, I., Westrip, J.R.S., Mueller, G.M., Martins-Cunha, K., Kirk, P., Tedersoo, L. & Antonelli, A. (2023) Pushing the frontiers of biodiversity research: Unveiling the global diversity, distribution, and conservation of fungi. Annual Review of Environment and Resources 48: 149–176. https://doi.org/10.1146/annurev-environ-112621-090937
  39. Nityananda, K., Sivasubramaniam, P. & Ajello, L. (1964) A case of mycotic keratitis caused by Curvularia geniculata. Archives of Ophthalmology 71: 456–458. https://doi.org/10.1001/archopht.1964.00970010472003
  40. Nyffeler, M. & Hywel-Jones, N. (2023) Diversity of spider families parasitized by fungal pathogens: A global review. BioRxiv 5: 1–79. https://doi.org/10.1101/2023.05.11.540451
  41. Priyadharsini, P. & Muthukumar, T. (2017) The root endophytic fungus Curvularia geniculata from Parthenium hysterophorus roots improves plant growth through phosphate solubilization and phytohormone production. Fungal Ecology 27: 69–77. https://doi.org/10.1016/j.funeco.2017.02.007
  42. Qi, Y., Fu, Y., Peng, J., Zeng, F., Wang, Y., Xie, Y. & Zhang, X. (2022) First report of banana (Musa acuminate cv. Formosana) Leaf spot disease caused by Curvularia geniculata in China. Plant Disease 106: 1758. https://doi.org/10.1094/PDIS-09-21-2001-PDN
  43. Rehner, S.A. & Buckley, E.A. (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
  44. 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
  45. Schmidt, V., Klasen, L., Schneider, J., Hübel, J. & Cramer, K. (2018) Pulmonary fungal granulomas and fibrinous pneumonia caused by different hypocrealean fungi in reptiles. Veterinary Microbiology 225: 58–63. https://doi.org/10.1016/j.vetmic.2018.09.008
  46. Shin, T.Y., Lee, M.R., Park, S.E., Lee, S.J., Kim, W.J. & Kim, J.S. (2020) Pathogenesis-related genes of entomopathogenic fungi. Archives of Insect Biochemistry and Physiology 105: e21747. https://doi.org/10.1002/arch.21747
  47. 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. Mycological Progress 18: 983–1003. https://doi.org/10.1007/s11557-019-01512-3
  48. Shrestha, B., Tanaka, E., Hyun, M.W., Han, J.G., Kim, C.S., Jo, J.W., Han, S.K., Oh, J., Sung, J.M. & Sung, G.H. (2017) Mycosphere essay 19. Cordyceps species parasitizing hymenopteran and hemipteran insects. Mycosphere 8: 1424–1442. https://doi.org/10.5943/mycosphere/8/9/8
  49. Shrestha, B., Zhang, W., Zhang, Y. & Liu, X. (2010) What is the Chinese caterpillar fungus Ophiocordyceps sinensis ()?. Mycology 1: 228–236. https://doi.org/10.1080/21501203.2010.536791
  50. Singh, S.M., Pathak, S.C., Kulkarni, N., Naidu, J. & Dubey, V. (1991) First report of phaeohyphomycosis of Nezara viridula Linn. (Insecta: Heteroptera) caused by Curvularia lunata. Mycopathologia 116: 37–43. https://doi.org/10.1007/BF00436088
  51. Spatafora, J.W., Quandt, C.A., Kepler, R.M., Sung, G.H., Shrestha, B., Hywel-Jones, N.L. & Luangsa-ard, J.J. (2015) New 1F1N species combinations in Ophiocordycipitaceae (Hypocreales). IMA Fungus 6: 357–362. https://doi.org/10.5598/imafungus.2015.06.02.07
  52. 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
  53. Sung, J.M. (1996) The insect-borne fungus of Korea in color (in Korean). Kyohak Publishing Co., Ltd. Seoul.
  54. Tan, Y.P., Crous, P.W. & Shivas, R.G. (2018) Cryptic species of Curvularia in the culture collection of the Queensland plant pathology herbarium. MycoKeys 35: 1–25. https://doi.org/10.3897/mycokeys.35.25665
  55. Tzean, S.S., Hsieh, L.S. & Wu, W.J. (1997) The genus Gibellula on spiders from Taiwan. Mycologia 89: 309–318. https://doi.org/10.1080/00275514.1997.12026787
  56. Verma, P., Singh, S. & Singh, R. (2013) Seven species of Curvularia isolated from three lakes of Bhopal. Advances in Life Science and Technology 8: 13–15.
  57. 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
  58. Wang, M., Zhou, H., Fu, Y. & Wang, C. (1996) The antifungal activities of the fungus 36-1 to several plant pathogens. Chinese Journal of Biological Control 12: 20–23.
  59. Wang, Z., Li, M., Ju, W., Ye, W., Xue, L., Boufford, D.E., Gao, X., Yue, B., Liu, Y. & Pierce, N.E. (2020) The entomophagous caterpillar fungus Ophiocordyceps sinensis is consumed by its lepidopteran host as a plant endophyte. Fungal Ecology 47: 100989. https://doi.org/10.1016/j.funeco.2020.100989
  60. White, T.J., Bruns, T., Lee, S.J.W.T. & 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. Academic Press, London, UK, pp. 315–322.https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  61. Xie, Y., Ying, J., Fang, L., Wu, J., Mao, X., Wang, L. & Wang, H. (2023) First report of Curvularia geniculata causing leave spot disease of Bletilla striata in Zhejiang of China. Plant Disease 107: 2527. https://doi.org/10.1094/PDIS-03-23-0407-PDN
  62. Yang, E.F., Tibpromma, S., Dai, D.Q., Promputtha, I., Mortimer, P.E. & Karunarathna, S.C. (2022) Three interesting fungal species associated with the Asian House Gecko in Kunming, China. Phytotaxa 545 (1): 37–56. https://doi.org/10.11646/phytotaxa.545.1.3
  63. Yoder, J.A., Fisher, K.A. & Dobrotka, C.J. (2018) A report on Purpureocillium lilacinum found naturally infecting the predatory mite, Balaustium murorum (Parasitengona: Erythraeidae). International Journal of Acarology 44: 139–145. https://doi.org/10.1080/01647954.2018.1487996
  64. Yousufi, M.K. (2023) The Hunt for Himalayan Traditional Medicine Parasitic Treasure: ‘Caterpillar Fungi’. Algerian Journal of Biosciences 4: 9–16. https://doi.org/10.57056/ajb.v4i1.104
  65. Zhaxybayeva, O. & Gogarten, J.P. (2002) Bootstrap, Bayesian probability and maximum likelihood mapping: Exploring new tools for comparative genome analyses. MBC Genomics 3: 1–15. https://doi.org/10.1186/1471-2164-3-4