Hesperomyces (Fungi, Ascomycota) associated with Hyperaspis ladybirds (Coleoptera, Coccinellidae): Rethinking host specificity
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
37746211
PubMed Central
PMC10512334
DOI
10.3389/ffunb.2022.1040102
Knihovny.cz E-zdroje
- Klíčová slova
- Coccinellidae, DNA barcoding, MCM7, arthropod-associated fungi, integrative taxonomy, nuclear ribosomal DNA, phylogeny,
- Publikační typ
- časopisecké články MeSH
Laboulbeniales (Ascomycota, Laboulbeniomycetes) are biotrophic microfungi always attached to the exoskeleton of their arthropod hosts. They do not form hyphae or a mycelium; instead, they undergo determinate growth, developing from a two-celled ascospore to form a multicellular thallus. Hesperomyces virescens has been reported on over 30 species of ladybirds (Coleoptera, Coccinellidae); in reality, it represents a complex of species, presumably segregated by host genus association. In this study, we report on Hesperomyces thalli on Hyperaspis vinciguerrae from the Canary Islands and compare them with the Hesperomyces hyperaspidis described on Hyperaspis sp. from Trinidad. We generated the sequences of the internal transcribed spacer (ITS) region, the large subunit (LSU) nuclear ribosomal RNA gene, and the minichromosome maintenance complex component 7 (MCM7) protein-coding gene. Our phylogenetic reconstruction of Hesperomyces based on a concatenated ITS-LSU-MCM7 dataset revealed Hesperomyces sp. ex Hy. vinciguerrae as a member of the He. virescens species complex distinct from He. virescens sensu stricto (s.s.). It also revealed that the Hesperomyces sp. ex Chilocorus bipustulatus from Algeria is different from He. virescens s.s., which is associated with Chilocorus stigma from the USA. This suggests that the species of Hesperomyces are not solely segregated by host association, but that there is also a biogeographical component involved. Based on these data, we refrained from referring our material from Hy. vinciguerrae to He. hyperaspidis. Finally, we discuss the usefulness of MCM7 as a useful marker for species delimitation in Hesperomyces.
Biology Centre of the Czech Academy of Sciences Institute of Entomology České Budějovice Czechia
Faculty of Science University of South Bohemia České Budějovice Czechia
Institute of Biological Sciences Cardinal Stefan Wyszyński University Warsaw Poland
Research Group Mycology Department of Biology Ghent University Ghent Belgium
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Abramoff M., Magalhães P., Ram S. J. (2004). Image processing with ImageJ. Biophotonics Int. 11, 36–42.
Bernardi M., Barragán A., Rossi W. (2014). New records of Laboulbeniales (Fungi: Ascomycota) from Ecuador and other countries. Webbia 69, 281–289. doi: 10.1080/00837792.2014.953369 DOI
Biedermann P., Vega F. (2020). Ecology and evolution of insect–fungus mutualisms. Annu. Rev. Entomol. 65, 431–455. doi: 10.1146/annurev-ento-011019-024910 PubMed DOI
Blackwell M., Haelewaters D., Pfister D. H. (2020). Laboulbeniomycetes: Evolution, natural history, and thaxter’s final word. Mycologia 112, 1048–1059. doi: 10.1080/00275514.2020.1718442 PubMed DOI
Bustamante D. E., Oliva M., Leiva S., Mendoza J. E., Bobadilla L., Angulo G., et al. . (2019). Phylogeny and species delimitations in the entomopathogenic genus Beauveria (Hypocreales, Ascomycota), including the description of B. peruviensis sp. nov. MycoKeys 58, 47–68. doi: 10.3897/mycokeys.58.35764 PubMed DOI PMC
Chernomor O., von Haeseler A., Minh B. Q. (2016). Terrace aware data structure for phylogenomic inference from supermatrices. Syst. Biol. 65, 997–1008. doi: 10.1093/sysbio/syw037 PubMed DOI PMC
Crous P. W., Osieck E. R., Jurjevi Ž, Boers J., Van Iperen A. L., Starink-Willemse M., et al. . (2021). Fungal planet description sheets: 1284–1382. Persoonia 47, 178–374. doi: 10.3767/persoonia.2021.47.06 PubMed DOI PMC
Goldmann L., Weir A. (2012). Position specificity in Chitonomyces (Ascomycota, Laboulbeniomycetes) on Laccophilus (Coleoptera, Dytiscidae): a molecular approach resolves a century-old debate. Mycologia 104, 1143–1158. doi: 10.3852/11-358 PubMed DOI
Goldmann L., Weir A., Rossi W. (2013). Molecular analysis reveals two new dimorphic species of Hesperomyces (Ascomycota, Laboulbeniomycetes) parasitic on the ladybird Coleomegilla maculata (Coleoptera, Coccinellidae). Fungal Biol. 117, 807–813. doi: 10.1016/j.funbio.2013.10.004 PubMed DOI
Haelewaters D., Blackwell M., Pfister D. H. (2021. a). Laboulbeniomycetes: Intimate fungal associates of arthropods. Annu. Rev. Entomol. 66, 257–276. doi: 10.1146/annurev-ento-013020-013553 PubMed DOI
Haelewaters D., De Kesel A. (2017). De schimmel Hesperomyces virescens, een natuurlijke vijand van lieveheersbeestjes. Entomol. Ber. 77, 106–118.
Haelewaters D., De Kesel A. (2020). Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including Hesperomyces halyziae and Laboulbenia quarantenae spp. nov. MycoKeys 71, 23–86. doi: 10.3897/mycokeys.71.53421 PubMed DOI PMC
Haelewaters D., De Kesel A., Gorczak M., Bao K., Gort G., Zhao S. Y., et al. . (2019. a). Laboulbeniales (Ascomycota) of the Boston Harbor Islands II (and other localities): Species parasitizing Carabidae, and the Laboulbenia flagellata species complex. Northeast. Nat. 25, 110–149. doi: 10.1656/045.025.s906 DOI
Haelewaters D., De Kesel A., Pfister D. H. (2018). Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Sci. Rep. 8, 15966. doi: 10.1038/s41598-018-34319-5 PubMed DOI PMC
Haelewaters D., Dima B., Abdel-Hafiz A., Abdel-Wahab M. A., Abul-Ezz S. R., Acar I., et al. . (2020). Fungal systematics and evolution: FUSE 6. Sydowia 72, 231–356. doi: 10.12905/0380.sydowia72-2020-0231 DOI
Haelewaters D., Gorczak M., Kaishian P., De Kesel A., Blackwell M. (2021. b). “Laboulbeniomycetes, enigmatic fungi with a turbulent taxonomic history,” in Encyclopedia of mycology, vol. 1 . Eds. Zaragoza Ó., Casadevall A. (Oxford: Elsevier; ), 263–283.
Haelewaters D., Gorczak M., Pfliegler W. P., Tartally A., Tischer M., Wrzosek M., et al. . (2015). Bringing Laboulbeniales to the 21st century: enhanced techniques for extraction and PCR amplification of DNA from minute ectoparasitic fungi. IMA Fungus 6, 363–372. doi: 10.5598/imafungus.2015.06.02.08 PubMed DOI PMC
Haelewaters D., Lubbers M., De Kesel A. (2022. a). The haustorium as a driving force for speciation in thallus-forming Laboulbeniomycetes. IMA Fungus 13, 1. doi: 10.1186/s43008-021-00087-7 PubMed DOI PMC
Haelewaters D., Pfister D. H. (2019). Morphological species of Gloeandromyces (Ascomycota, Laboulbeniales) evaluated using single-locus species delimitation methods. Fungal Syst. Evol. 3, 19–34. doi: 10.3114/fuse.2019.03.03 PubMed DOI PMC
Haelewaters D., Pfliegler W. P., Gorczak M., Pfister D. H. (2019. b). Birth of an order: Comprehensive molecular phylogenetic study excludes Herpomyces (Fungi, Laboulbeniomycetes) from Laboulbeniales. Mol. Phylogenet. Evol. 133, 286–301. doi: 10.1016/j.ympev.2019.01.007 PubMed DOI
Haelewaters D., Rossi W. (2015). Three new species of Laboulbenia from Roland Thaxter’s backlog of slides and a brief review of Laboulbeniales associated with Chrysomelidae. Mycologia 107, 142–148. doi: 10.3852/14-022 PubMed DOI
Haelewaters D., Van Caenegem W., De Kesel A. (2022. b). Hesperomyces harmoniae, a new name for a common ectoparasitic fungus on the invasive alien ladybird Harmonia axyridis . Sydowia 75, 53–74. doi: 10.12905/0380.sydowia75-2023-0053 DOI
Hall T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.
Hoang D. T., Chernomor O., von Haeseler A., Minh B. Q., Vinh L. S. (2018). UFBoot2: Improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522. doi: 10.1093/molbev/msx281 PubMed DOI PMC
Hopple J. S. (1994). Phylogenetic investigations in the genus Coprinus based on morphological and molecular characters. Ph.D. dissertation (Durham, NC: Duke University; ).
Kalyaanamoorthy S., Minh B., Wong T., von Haeseler A., Jermiin L. (2017). ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589. doi: 10.1038/nmeth.4285 PubMed DOI PMC
Katoh K., Rozewicki J., Yamada K. D. (2019). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 20, 1160–1166. doi: 10.1093/bib/bbx108 PubMed DOI PMC
Kuraku S., Zmasek C. M., Nishimura O., Katoh K. (2013). aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res. 41, W22–W28. doi: 10.1093/nar/gkt389 PubMed DOI PMC
Liu J., Haelewaters D., Pfliegler W. P., Page R. A., Dick C. W., Aime M. C. (2020). A new species of Gloeandromyces from Ecuador and Panama revealed by morphology and phylogenetic reconstruction, with a discussion of secondary barcodes in Laboulbeniomycetes taxonomy. Mycologia 112, 1192–1202. doi: 10.1080/00275514.2020.1781496 PubMed DOI
Nguyen L.-T., Schmidt H. A., von Haeseler A., Minh B. Q. (2015). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274. doi: 10.1093/molbev/msu300 PubMed DOI PMC
Romanowski J., Ceryngier P., Větrovec J., Szawaryn K. (2019). The Coccinellidae (Coleoptera) from Fuerteventura, Canary Islands. Zootaxa 4646, 101–123. doi: 10.11646/zootaxa.4646.1.6 PubMed DOI
Schmitt I., Crespo A., Divakar P. K., Fankhauser J. D., Herman-Sackett E., Kalb K., et al. . (2009). New primers for promising single-copy genes in fungal phylogenetics and systematics. Persoonia 23, 35–40. doi: 10.3767/003158509X470602 PubMed DOI PMC
Schoch C. L., Seifert K. A., Huhndorf S., Robert V., Spouge J. L., Levesque C. A., et al. . (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. U.S.A. 109, 6241–6246. doi: 10.1073/pnas.1117018109 PubMed DOI PMC
Sundberg H., Kruys Å., Bergsten J., Ekman S. (2018). Position specificity in the genus Coreomyces (Laboulbeniomycetes, Ascomycota). Fungal Syst. Evol. 1, 217–228. doi: 10.3114/fuse.2018.01.09 PubMed DOI PMC
Thaxter R. (1891). Supplementary note on North American Laboulbeniaceae. Proc. Am. Acad. Arts Sci. 25, 261–270. doi: 10.2307/20020441 DOI
Thaxter R. (1931). Contribution towards a monograph of the Laboulbeniaceae. Part V. Mem. Am. Acad. Arts Sci. 16, 7–435. doi: 10.2307/25058136 DOI
Vaidya G., Lohman D. J., Meier R. (2011). SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171–180. doi: 10.1111/j.1096-0031.2010.00329.x PubMed DOI
Vilgalys R., Hester M. (1990). Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 172, 4238–4246. doi: 10.1128/jb.172.8.4238-4246.1990 PubMed DOI PMC
Walker M. J., Dorrestein A., Camacho J. J., Meckler L. A., Silas K. A., Hiller T., et al. . (2018). A tripartite survey of hyperparasitic fungi associated with ectoparasitic flies on bats (Mammalia: Chiroptera) in a neotropical cloud forest in Panama. Parasite 25, 19. doi: 10.1051/parasite/2018017 PubMed DOI PMC