Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2024-03-28
Page range: 127-140
Abstract views: 1
PDF downloaded: 0

Phylogenetic and taxonomic appraisal of Neomanoharachariella xizangensis sp. nov. and the first asexual report of Acanthostigmina (Tubeufiaceae, Tubeufiales) from Xizang Autonomous Region, China

CAS Key Laboratory for Plant Diversity and Biogeography of East Asia; Kunming Institute of Botany; Chinese Academy of Sciences; Panlong District; Kunming; Yunnan; 650201; P. R. China; Center of Excellence in Fungal Research; Mae Fah Luang University; Chiang Rai 57100; Thailand; School of Science; Mae Fah Luang University; Chiang Rai 57100; Thailand
CAS Key Laboratory for Plant Diversity and Biogeography of East Asia; Kunming Institute of Botany; Chinese Academy of Sciences; Panlong District; Kunming; Yunnan; 650201; P. R. China
Honghe Center for Mountain Futures; Kunming Institute of Botany; Chinese Academy of Sciences; Honghe County 654400; Yunnan Province; P.R. China
Center of Excellence in Fungal Research; Mae Fah Luang University; Chiang Rai 57100; Thailand
CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Panlong District, Kunming, Yunnan, 650201, P. R. China
1 new species geographical record helicosporous hyphomycetes multigene phylogeny muriform, saprobe terrestrial Fungi

Abstract

Tubeufiaceae species have diverse morphologies and habitats and are distributed in both tropical and temperate regions. In the past decade, several new and interesting Tubeufiaceae species were reported from China in aquatic and terrestrial habitats. In this study, we investigated two saprobic species collected on decaying wood in a terrestrial habitat of Xizang Autonomous Region, China. Through phylogenetic analyses of a combined ITS, LSU, tef1-α, and rpb2 dataset coupled with detailed morphological examinations, a novel species within Neomanoharachariella was identified. Phylogenetic analyses revealed that this new species formed a sister clade to Neomanoharachariella aquatica, but can be morphologically distinguished by its pale brown, septate, and flexuous conidiophores, alongside dark brown setae that turn hyaline at the apex and distinct muriform conidia. In addition, this study presents the first asexual and geographical record of Acanthostigmina (A. multiseptatum) from China. Acanthostigmina multiseptatum is characterized by micronematous, hyaline, and septate conidiophores with unique pleurogenous and helicoid conidia.

References

  1. Barr, M.E. (1979) A classification of Loculoascomycetes. Mycologia 71 (5): 935–957. https://doi.org/10.1080/00275514.1979.12021099
  2. Bezerra, J.D., Oliveira, R.J., Paiva, L.M., Silva, G.A., Groenewald, J.Z., Crous, P.W. & Souza-Motta, C.M. (2017) Bezerromycetales and Wiesneriomycetales ord. nov. (class Dothideomycetes), with two novel genera to accommodate endophytic fungi from Brazilian cactus. Mycological Progress 16: 297–309. https://doi.org/10.1007/s11557-016-1254-0
  3. Boonmee, S., Rossman, A.Y., Liu, J.K., Li, W.J., Dai, D.Q., Bhat, J.D., Jones, E.G., McKenzie, E.H., Xu, J.C. & Hyde, K.D. (2014) Tubeufiales, ord. nov., integrating sexual and asexual generic names. Fungal Diversity 68: 239–298. https://doi.org/10.1007/s13225-014-0304-7
  4. Boonmee, S., Zhang, Y., Chomnunti, P., Chukeatirote, E., Tsui, C.K., Bahkali, A.H. & Hyde, K.D. (2011) Revision of lignicolous Tubeufiaceae based on morphological reexamination and phylogenetic analysis. Fungal Diversity 51: 63–102. https://doi.org/10.1007/s13225-011-0147-4
  5. Brahamanage, R.S., Lu, Y.Z., Bhat, D.J., Wanasinghe, D.N., Yan, J.Y., Hyde, K.D. & Boonmee, S. (2017) Phylogenetic investigations on freshwater fungi in Tubeufiaceae (Tubeufiales) reveals the new genus Dictyospora and new species Chlamydotubeufia aquatica and Helicosporium flavum. Mycosphere 8: 917–933 https://doi.org/10.5943/mycosphere/8/7/8
  6. Cai, L., Tsui, C.K.M., Zhang, K.Q. & Hyde, K.D. (2002) Aquatic fungi from Lake Fuxian, Yunnan, China. Fungal Diversity 9: 57–70.
  7. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular biology and evolution 17 (4): 540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
  8. Chaiwan, N., Lu, Y.Z., Tibpromma, S., Bhat, D.J., Hyde, K.D. & Boonmee, S. (2017) Neotubeufia gen. nov. and Tubeufia guangxiensis sp. nov. (Tubeufiaceae) from freshwater habitats. Mycosphere 8: 1443–1456. https://doi.org/10.5943/mycosphere/8/9/9
  9. Chethana, K.T., Manawasinghe, I.S., Hurdeal, V.G., Bhunjun, C.S., Appadoo, M.A., Gentekaki, E., Raspé, O., Promputtha, I. & Hyde, K.D. (2021) What are fungal species and how to delineate them?. Fungal Diversity 109 (1): 1–25. https://doi.org/10.1007/s13225-021-00483-9
  10. Chomnunti, P., Hongsanan, S., Aguirre-Hudson, B., Tian, Q., Persoh, D., Dhami, M.K., Alias, A.S., Xu, J., Liu, X., Stadler, M. & Hyde, K.D. (2014) The sooty moulds. Fungal Diversity 66: 1–36. https://doi.org/10.1007/s13225-014-0278-5
  11. Corda, A.C.J. (1837) Icones fungorum hucusque cognitorum, vol 1. J. G. Calve, Prague, pp. 1–32.
  12. Clewley, J.P. (1995) Macintosh sequence analysis software. Molecular biotechnology 3: 221–224. https://doi.org/10.1007/BF02789332
  13. Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and high-performance computing. Nature methods 9 (8): 772. https://doi.org/10.1038/nmeth.2109
  14. Dong, W., Wang, B., Hyde, K.D., McKenzie, E.H., Raja, H.A., Tanaka, K., Abdel-Wahab, M.A., Abdel-Aziz, F.A., Doilom, M., Phookamsak, R. & Hongsanan, S. (2020) Freshwater dothideomycetes. Fungal Diversity 105: 319–575. https://doi.org/10.1007/s13225-020-00463-5
  15. Fan, C., Lu, Y., Kang, J., Wang, L., Lei, B. & Chen, L. (2019) Bioactivity evaluation of secondary metabolites produced by species of Tubeufiaceae. Mycosystema 38 (4): 560–74. https://doi.org/10.13346/j.mycosystema.180316
  16. Goos, R.D. (1985) A review of the anamorph genus Helicomyces. Mycologia 77: 606–618. https://doi.org/10.1080/00275514.1985.12025146
  17. Goos, R.D. (1986) A review of the anamorph genus Helicoma. Mycologia 78: 744–761. https://doi.org/10.1080/00275514.1986.12025318
  18. Goos, R.D. (1989) On the anamorph genera Helicosporium and Drepanospora. Mycologia 81: 356–374. https://doi.org/10.1080/00275514.1989.12025759
  19. Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic biology 52 (5): 696–704. https://doi.org/10.1080/10635150390235520
  20. Hanada, T., Sato, T., Arioka, M., Uramoto, M. & Yamasaki, M. (1996) Purification and characterization of a 15 kDa Protein (p15) produced by Helicosporium that exhibits distinct effects on Neurite Outgrowth from Cortical Neurons and PC12 cells. Biochemical and biophysical research communications 228 (1): 209–215. https://doi.org/10.1006/bbrc.1996.1641
  21. HF, L. (1809) Observationes in ordines plantarum naturales. Dissertatio I. Mag Ges Naturf Freunde Berlin 3: 3–42.
  22. Hongsanan, S., Hyde, K.D., Phookamsak, R., Wanasinghe, D.N., McKenzie, E.H., Sarma, V.V., Lücking, R., Boonmee, S., Bhat, J.D., Liu, N.G. & Tennakoon, D.S. (2020) Refined families of Dothideomycetes: Orders and families incertae sedis in Dothideomycetes. Fungal Diversity 105: 17–318. https://doi.org/10.1007/s13225-020-00462-6
  23. Hu, D.M., Liu, F. & Cai, L. (2013) Biodiversity of aquatic fungi in China. Mycology 4 (3): 125–168. https://doi.org/10.1080/21501203.2013.835752
  24. Hua, Z., Lv, Q., Ye, W., Wong, C.K.A., Cai, G., Gu, D., Ji, Y., Zhao, C., Wang, J., Yang, B.B. & Zhang, Y. (2006) MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PloS one 1 (1): e116. https://doi.org/10.1371/journal.pone.0000116
  25. Hyde, K.D., Norphanphoun, C., Abreu, V.P., Bazzicalupo, A., Thilini Chethana, K.W., Clericuzio, M., Dayarathne, M.C., Dissanayake, A.J., Ekanayaka, A.H., He, M.Q. & Hongsanan, S. (2017) Fungal diversity notes 603–708: taxonomic and phylogenetic notes on genera and species. Fungal Diversity 87: 1–235. https://doi.org/10.1007/s13225-017-0391-3
  26. Hyde, K.D., Hongsanan, S., Jeewon, R., Bhat, D.J., McKenzie, E.H., Jones, E.B., Phookamsak, R., Ariyawansa, H.A., Boonmee, S., Zhao, Q. & Abdel-Aziz, F.A. (2016b) Fungal diversity notes 367–490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity 80 (1): 1–270. https://doi.org/10.1007/s13225-016-0373-x
  27. Itazaki, H., Nagashima, K., Sugita, K., Yoshida, H., Kawamura, Y., Yasuda, Y., Matsumoto, K., Ishii, K., Uotani, N., Nakai, H. & Terui A. (1990) Solation and structural elucidation of new cyclotetrapeptides, trapoxins A and B, having detransformation activities as antitumor agents. The Journal of antibiotics 43 (12): 1524–1532. https://doi.org/10.7164/antibiotics.43.1524
  28. Jayasiri, S.C., Hyde, K.D., Ariyawansa, H.A., Bhat, J., Buyck, B., Cai, L., Dai, Y.C., Abd-Elsalam, K.A., Ertz, D., Hidayat, I. & Jeewon, R. (2015) The faces of fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal diversity 74: 3–18. https://doi.org/10.1007/s13225-015-0351-8
  29. Jeewon, R. & Hyde, K.D. (2016) Establishing species boundaries and new taxa among fungi: recommendations to resolve taxonomic ambiguities. Mycosp 7 (11): 1669–77. https://doi.org/10.5943/mycosphere/7/11/4
  30. Kirk, P.M., Cannon, P.F., David, J.C. & Stalpers, J.A. (2001) Ainsworth & Bisby’s Dictionary of the Fungi, 9th ed.. CABI International: Wallingford, UK, pp. 1–655.
  31. Li, L.L., Shen, H.W., Bao, D.F., Wanasinghe, D.N., Lu, Y.Z., Feng, Y. & Luo, Z.L. (2022) The plethora of Tubeufiaceae in lakes of the northwestern Yunnan plateau, China. Frontiers in Microbiology 13: 1056669. https://doi.org/10.3389/fmicb.2022.1056669
  32. Link, J.H.F. (1809) Observationes in ordines plantarum naturales. Dissertatio Ima. Gesellschaft Naturforschender Freundezu Berlin, Magazin 3 (1): 3–42.
  33. Liu, J.K., Lu, Y.Z., Cheewangkoon, R. & To-Anun, C. (2018) Phylogeny and morphology of Helicotubeufia gen. nov, with three new species in Tubeufiaceae from aquatic habitats. Mycosphere: 495–509. https://doi.org/10.5943/mycosphere/9/3/4
  34. Liu, J.K., Hyde, K.D., Jeewon, R., Phillips, A.J., Maharachchikumbura, S.S., Ryberg, M., Liu, Z.Y. & Zhao, Q. (2017) Ranking higher taxa using divergence times: a case study in Dothideomycetes. Fungal Diversity 84: 75–99. https://doi.org/10.1007/s13225-017-0385-1
  35. Lu, Y.Z., Boonmee, S., Bhat, D.J., Hyde, K.D. & Kang, J.C. (2017a) Helicosporium luteosporum sp. nov. and Acanthohelicospora aurea (Tubeufiaceae, Tubeufiales) from terrestrial habitats. Phytotaxa 319 (3): 241–53. https://doi.org/10.11646/phytotaxa.319.3.3
  36. Lu, Y.Z., Boonmee, S., Dai, D.Q., Liu, J.K., Hyde, K.D., Bhat, D.J., Ariyawansa, H. & Kang, J.C. (2017b) Four new species of Tubeufia (Tubeufiaceae, Tubeufiales) from Thailand. Mycological Progress 16: 403–417. https://doi.org/10.1007/s11557-017-1280-6
  37. Lu, Y.Z., Boonmee, S., Liu, J.K., Hyde, K.D., McKenzie, E.H., Eungwanichayapant, P.D. & Kang, J.C. (2018a) Multigene phylogenetic analyses reveal Neohelicosporium gen. nov. and five new species of helicosporous hyphomycetes from aquatic habitats. Mycological Progress 17: 631–46. https://doi.org/10.1007/s11557-017-1366-1
  38. Lu, Y.Z., Liu, J.K., Hyde, K.D., Jeewon, R., Kang, J.C., Fan, C., Boonmee, S., Bhat, D.J., Luo, Z.L., Lin, C.G. & Eungwanichayapant, P.D. (2018b) A taxonomic reassessment of Tubeufiales based on multi-locus phylogeny and morphology. Fungal Diversity 92: 131–344. https://doi.org/10.1007/s13225-018-0411-y
  39. Lumbsch, H.T. & Huhndorf, S.M. (2010) Myconet volume 14. Part one. Outline of Ascomycota—2009. Part two. Notes on ascomycete systematics. Nos. 4751–5113. Fieldiana Life and Earth Sciences 2010 (1): 1–64. https://doi.org/10.3158/1557.1
  40. Luo, J., Yin, J., Cai, L., Zhang, K. & Hyde, K.D. (2004) Freshwater fungi in Lake Dianchi, a heavily polluted lake in Yunnan, China. Fungal Diversity 16: 93–112.
  41. Luo, Z.L., Bhat, D.J., Jeewon, R., Boonmee, S., Bao, D.F., Zhao, Y.C., Chai, H.M., Su, H.Y., Su, X.J. & Hyde, K.D. (2017) Molecular phylogeny and morphological characterisation of asexual fungi (Tubeufiaceae) from freshwater habitats in Yunnan, China. Cryptogam Mycol 38: 27–53. https://doi.org/10.7872/crym/v38.iss1.2017.27
  42. Ma, J., Xiao, X.J., Liu, N.G., Boonmee, S., Xiao, Y.P. & Lu, Y.Z. (2023) Morphological and multigene phylogenetic analyses reveal Pseudotubeufia gen. nov. and two new species in Tubeufiaceae from China. Journal of Fungi 9 (7): 742. https://doi.org/10.3390/jof9070742
  43. Maharachchikumbura, S.S., Chen, Y., Ariyawansa, H.A., Hyde, K.D., Haelewaters, D., Perera, R.H., Samarakoon, M.C., Wanasinghe, D.N., Bustamante, D.E., Liu, J.K. & Lawrence, D.P. (2021) Integrative approaches for species delimitation in Ascomycota. Fungal Diversity 109 (1): 155–179. https://doi.org/10.1007/s13225-021-00486-6
  44. Mao, Z.L., Sun, W.B., Fu, L.Y., Luo, H.Y., Lai, D.W. & Zhou, L.G. (2014) Natural dibenzo-α-pyrones and their bioactivities. Molecules 19 (4): 5088–5108. https://doi.org/10.3390/molecules19045088
  45. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2012) The CIPRES science gateway: enabling high-impact science for phylogenetics researchers with limited resources. Proceedings of the 1st Conference of the Extreme Science and Engineering Discovery Environment: Bridging from the extreme to the campus and beyond, pp. 1–8. https://doi.org/10.1145/2335755.2335836
  46. Nees Von Esenbeck, C.G.D. (1817) System der Pilze und Schwa¨mme Wu¨rtzburg. pp. 1–334.
  47. Phookamsak, R., Lu, Y.Z., Hyde, K.D., Jeewon, R., Li, J.F., Doilom, M., Boonmee, S. & Promputtha, I. (2018) Phylogenetic characterisation of two novel Kamalomyces species in Tubeufiaceae (Tubeufiales). Mycological Progress 17: 647–660. https://doi.org/10.1007/s11557-017-1365-2
  48. Promputtha, I. & Miller, A.N. (2010) Three new species of Acanthostigma (Tubeufiaceae, Dothideomycetes) from Great Smoky Mountains National Park. Mycologia 102 (3): 574–587. https://doi.org/10.3852/09-051
  49. Qian, S.Y., Zeng, X.B., Qian, Y.X., Lu, Y.Z., He, Z.J. & Kang, J.C. (2023) A saprophytic fungus Tubeufia rubra produces novel rubracin D and E reversing multidrug resistance in cancer cells. Journal of Fungi 9 (3): 309. https://doi.org/10.3390/jof9030309
  50. Rannala, B. & Yang, Z. (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. Journal of molecular evolution 43: 304–311. https://doi.org/10.1007/BF02338839
  51. 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 (3): 539–42. https://doi.org/10.1093/sysbio/sys029
  52. Rossman, A.Y. (1987) The Tubeufiaceae and similar loculoascomycetes. Mycological Papers 157: 1–71.
  53. Saccardo, P.A. (1883) Sylloge Fungorum. Patavii Ital 2: 1–815.
  54. Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (9): 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  55. Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic biology 56 (4): 564–577. https://doi.org/10.1080/10635150701472164
  56. Tian, X., Karunarathna, S.C., Xu, R., Lu, Y., Suwannarach, N., Mapook, A., Bao, D., Xu, J. & Tibpromma, S. (2022) Three new species, two new records and four new collections of Tubeufiaceae from Thailand and China. Journal of Fungi 8 (2): 206. https://doi.org/10.3390/jof8020206
  57. Von Höhnel, F. (1909) Fragmente zur Mykologie. XV. Mitteilung, Nr. 407 bis 467. Math Naturw Kl, Abt 1: 1461–1552.
  58. Wijayawardene, N.N., Hyde, K.D., Dai, D.Q., Sánchez-García, M., Goto, B.T. & Magurno, F. (2022) Outline of Fungi and fungus-like taxa. Mycosphere 13 (1): 53–453. https://doi.org/10.5943/mycosphere/13/1/2
  59. Xiao, X.J., Ma, J., Zhang, L.J., Liu, N.G., Xiao, Y.P., Tian, X.G., Luo, Z.L. & Lu, Y.Z. (2023) Additions to the genus Helicosporium (Tubeufiaceae, Tubeufiales) from China with an identification key to Helicosporium taxa. Journal of Fungi 9 (7): 775. https://doi.org/10.20944/preprints202306.1515.v1
  60. Zeng, X., Qian, S., Lu, Y., Li, Y., Chen, L., Qian, Y., He, Z. & Kang, J. (2022) A novel Nitrogen-containing Glyceride from fungal saprobe Tubeufia rubra reverses MDR of tumor cell lines to Doxorubicin. Records of Natural Products 16: 622–632. https://doi.org/10.25135/rnp.320.2201.2334
  61. Zhang, L.J., Yang, M.F., Ma, J., Xiao, X.J., Ma, X.Y., Zheng, D.G., Han, M.Y., Xia, M.L., Jayawardena, R.S., Mapook, A. & Xiao, Y.P. (2023) Neogrisphenol A, a potential ovarian cancer inhibitor from a new record fungus Neohelicosporium griseum. Metabolites 13 (3): 435. https://doi.org/10.3390/metabo13030435
  62. Zhaxybayeva, O. & Gogarten, J.P. (2002) Bootstrap, Bayesian probability and maximum likelihood mapping: exploring new tools for comparative genome analyses. BMC genomics 3 (1): 1–5. https://doi.org/10.1186/1471-2164-3-4
  63. Zheng, W., Han, L., He, Z.J. & Kang, J.C. (2023) A new alkaloid derivative from the saprophytic fungus Neohelicomyces hyalosporus PF11–1. Natural Product Research 9: 1–5. https://doi.org/10.1080/14786419.2023.2167202