Abstract
The Arthrodermataceae, or dermatophytes, are a major family in the Onygenales and important from a public health safety perspective. Here, based on sequenced and downloaded from GenBank sequences, the evolutionary relationships of Arthrodermataceae were comprehensively studied via phylogenetic reconstruction, divergence time estimation, phylogenetic split network, and phylogeography analysis. These results showed the clades Ctenomyces, Epidermophyton, Guarromyces, Lophophyton, Microsporum, Paraphyton, and Trichophyton were all monophyletic groups, whereas Arthroderma and Nannizzia were polyphyletic. Among them, Arthroderma includes at least four different clades, Arthroderma I, III and IV are new clades in Arthrodermataceae. Nannizzia contains at least two different clades, Nannizzia I and Nannizzia II, but Nannizzia II was a new clade in Arthrodermataceae. The unclassified group, distributed in Japan and India, was incorrectly identified; it should be a new clade in Arthrodermataceae. The phylogenetic split network based on the ITS sequences provided strong support for the true relationships among the lineages in the reconstructed phylogenetic tree. A haplotype phylogenetic network based on the ITS sequences was used to visualize species evolution and geographic lineages relationships in all genera except Trichophyton. The new framework provided here for the phylogeny and taxonomy of Arthrodermataceae will facilitate the rapid identification of species in the family, which should useful for evaluating the results of preventive measures and interventions, as well as for conducting epidemiological studies.
Similar content being viewed by others
Data Availability
The datasets analysed during the current study are available in the GenBank (ITS: MZ019572, MZ019566–MZ020153; LSU: MZ019553–MZ019565; RP 60S L1: OK448405–OK448417; TEF3: OK448392–OK448404; TUB2: OK448379–OK448391).
References
Baert F, Stubbe D, D’hooge E, Packeu A, Hendrickx M (2020) Updating the taxonomy of dermatophytes of the BCCM/IHEM collection according to the new standard: a phylogenetic approach. Mycopathologia 185:161–168. https://doi.org/10.1007/s11046-019-00338-7
Bakkes DK, Chitimia-Dobler L, Matloa D, Oosthuysen M, Mumcuoglu KY, Mans BJ, Matthee CA (2020) Integrative taxonomy and species delimitation of Rhipicephalus turanicus (Acari: Ixodida: Ixodidae). Int J Parasitol 50:577–594. https://doi.org/10.1016/j.ijpara.2020.04.005
Balvočiūtė M, Spillner A, Moulton V (2014) FlatNJ: a novel network-based approach to visualize evolutionary and biogeographical relationships. Syst Biol 63:383–396. https://doi.org/10.1093/sysbio/syu001
Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Banerjee S, Walder F, Büchi L, Meyer M, Held AY, Gattinger A, Keller T, Charles R, van der Heijden MGA (2019) Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J 13:1722–1736. https://doi.org/10.1038/s41396-019-0383-2
Bapteste E, van Iersel L, Janke A, Kelchner S, Kelk S, McInerney JO, Morrison DA, Nakhleh L, Steel M, Stougie L, Whitfield J (2013) Networks: expanding evolutionary thinking. Trends Genet 29:439–441. https://doi.org/10.1016/j.tig.2013.05.007
Begum J, Kumar K (2021) Prevalence of dermatophytosis in animals and antifungal susceptibility testing of isolated Trichophyton and Microsporum species. Trop Anim Health pro 53:3. https://doi.org/10.1007/s11250-020-02476-3
Begum J, Mir NA, Lingaraju MC, Buyamayum B, Dev K (2020) Recent advances in the diagnosis of dermatophytosis. J Basic Microb 60:293–303. https://doi.org/10.1002/jobm.201900675
Brewer MT, Cameron CJ, Chan CT, Dutta B, Gitaitis R, Grauke LJ, Brock JH, Brenneman TB (2021) Neofusicoccum caryigenum, a new species causing leaf dieback disease of pecan (Carya illinoinensis). Mycologia 113:586–598. https://doi.org/10.1080/00275514.2021.1880216
Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265. https://doi.org/10.1093/molbev/msh018
Carrascal-Correa DF, Zuluaga A, González A (2020) Species distribution of the main aetiologic agents causing skin dermatophytosis in Colombian patients: a 23-year experience at a mycological reference center. Mycoses 63:494–499. https://doi.org/10.1111/myc.13073
Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chen L, Li H, Jiao W, Tao M, Lv C, Zhao M, Wang M (2021) Genetic variation and demographic history analysis of Pestalotiopsis, Pseudopestalotiopsis, and Neopestalotiopsis fungi associated with tea (Camellia sinensis) inferred from the internal transcribed spacer region of the nuclear ribosomal DNA. Plant Pathol 70:699–711. https://doi.org/10.1111/ppa.13315
Čmoková A, Kolařík M, Dobiáš R, Hoyer LL, Janouškovcová H, Kano R, Kano I, Lysková P, Machová L, Maier T, Mallátová N, Man M, Mencl K, Nenoff P, Peano A, Prausová H, Stubbe D, Uhrlaß S, Větrovský T, Wiegand C, Hubka V (2021) Resolving the taxonomy of emerging zoonotic pathogens in the Trichophyton benhamiae complex. Fungal Divers 104:333–387. https://doi.org/10.1007/s13225-020-00465-3
Dai YD, Wu CK, Yuan F, Wang YB, Huang LD, Chen ZH, Zeng WB, Wang Y, Yang ZL, Zeng PS, Lemetti P, Mo XX, Yu H (2020) Evolutionary biogeography on Ophiocordyceps sinensis: an indicator of molecular phylogeny to geochronological and ecological exchanges. Geosci Front 11:807–820. https://doi.org/10.1016/j.gsf.2019.09.001
de Wit R, Bouvier T (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8:755–758. https://doi.org/10.1111/j.1462-2920.2006.01017.x
de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hendrickx M, Kupsch C, Stielow JB, Freeke J, Göker M, Rezaei-Matehkolaei A, Mirhendi H, Gräser Y (2017) Toward a novel multilocus phylogenetic taxonomy for the dermatophytes. Mycopathologia 182:5–31. https://doi.org/10.1007/s11046-016-0073-9
De Luca D, Piredda R, Sarno D, Kooistra WHCF (2021) Resolving cryptic species complexes in marine protists: phylogenetic haplotype networks meet global DNA metabarcoding datasets. ISME J 15:1931–1942. https://doi.org/10.1038/s41396-021-00895-0
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88. https://doi.org/10.1371/journal.pbio.0040088
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075
Dukik K, de Hoog GS, Stielow JB, Freeke J, van den Ende BG, Vicente VA, Menken SBJ, Ahmed SA (2020) Molecular and phenotypic characterization of Nannizzia (Arthrodermataceae). Mycopathologia 185:9–35. https://doi.org/10.1007/s11046-019-00336-9
Estensmo ELF, Maurice S, Morgado L, Martin-Sanchez PM, Skrede I, Kauserud H (2021) The influence of intraspecific sequence variation during DNA metabarcoding: a case study of eleven fungal species. Mol Ecol Resour 21:1141–1148. https://doi.org/10.1111/1755-0998.13329
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Georges-Filteau J, Hamelin RC, Blanchette M (2020) Mycorrhiza: genotype assignment using phylogenetic networks. Bioinformatics 36:212–220. https://doi.org/10.1093/bioinformatics/btz476
Gordon AK, McIver C, Kim M, Murrell DF, Taylor P (2016) Clinical application of a molecular assay for the detection of dermatophytosis and a novel non-invasive sampling technique. Pathology 48:720–726. https://doi.org/10.1016/j.pathol.2016.08.006
Haelewaters D, Pfliegler WP, Gorczak M, Pfister DH (2019) Birth of an order: comprehensive molecular phylogenetic study excludes Herpomyces (Fungi, Laboulbeniomycetes) from Laboulbeniales. Mol Phylogenet Evol 113:286–301. https://doi.org/10.1016/j.ympev.2019.01.007
Hainsworth S, Kučerová I, Sharma R, Cañete-Gibas CF, Hubka V (2020) Three-gene phylogeny of the genus Arthroderma: basis for future taxonomic studies. Med Mycol, pp 1–11. https://doi.org/10.1093/mmy/myaa057
Huson DH, Kloepper TH (2005) Computing recombination networks from binary sequences. Bioinformatics 21:ii159–ii165. https://doi.org/10.1093/bioinformatics/bti1126
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030
Hyde KD, Maharachchikumbura SSN, Hongsanan S, Samarakoon MC, Lücking R, Pem D, Harishchandra D, Jeewon R, Zhao RL, Xu JC, Liu JK, Al-Sadi A, Bahkali AH, Elgorban AM (2017) The ranking of fungi: a tribute to David L. Hawksworth on his 70th birthday. Fungal Divers 84:1–23. https://doi.org/10.1007/s13225-017-0383-3
James TY, Stajich JE, Hittinger CT, Rokas A (2020) Toward a fully resolved fungal tree of life. Annu Rev Microbiol 74:291–313. https://doi.org/10.1146/annurev-micro-022020-051835
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kennedy M, Holland BR, Gray RD, Spencer HG (2005) Untangling long branches: identifying conflicting phylogenetic signals using spectral analysis, neighbor-net, and consensus networks. Syst Biol 54:620–633. https://doi.org/10.1080/106351591007462
Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Mardulyn P (2012) Trees and/or networks to display intraspecific DNA sequence variation? Mol Ecol 21:3385–3390. https://doi.org/10.1111/j.1365-294X.2012.05622.x
Minh Q, Nguyen M, von Haeseler AA (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195. https://doi.org/10.1093/molbev/mst024
Morrison DA (2005) Networks in phylogenetic analysis: new tools for population biology. Int J Parasitol 35:567–582. https://doi.org/10.1016/j.ijpara.2005.02.007
Morrison DA (2014) Is the tree of life the best metaphor, model, or heuristic for phylogenetics? Syst Biol 63:628–638. https://doi.org/10.1093/sysbio/syu026
Nakhleh L, Warnow T, Linder CR, John KS (2005) Reconstructing reticulate evolution in species-theory and practice. J Comput Biol 12:796–811. https://doi.org/10.1089/cmb.2005.12.796
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson K-H (2008) Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinform 4:193–201
Pardi F, Scornavacca C (2015) Reconstructible phylogenetic networks: do not distinguish the indistinguishable. PLoS Comput Biol 11:e1004135. https://doi.org/10.1371/journal.pcbi.1004135
Prieto M, Wedin M (2013) Dating the diversification of the major lineages of Ascomycota (Fungi). PLoS ONE 8:e65576. https://doi.org/10.1371/journal.pone.0065576
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Riccioni C, Rubini A, Türkoğlu A, Belfiori B, Paolocci F (2019) Ribosomal DNA polymorphisms reveal genetic structure and a phylogeographic pattern in the Burgundy truffle Tuber aestivum Vittad. Mycologia 111:26–39. https://doi.org/10.1080/00275514.2018.1543508
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Shapiro BJ, Leducq J-B, Mallet J (2016) What is speciation? PLoS Genet 12:e1005860. https://doi.org/10.1371/journal.pgen.1005860
Szczepańska K, Guzow-Krzemińska B, Urbaniak J (2021) Infraspecific variation of some brown Parmeliae (in Poland)—a comparison of ITS rDNA and non-molecular characters. MycoKeys 85:127–160. https://doi.org/10.3897/mycokeys.85.70552
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Yakahashi K, Sugiyama K, Hiruma M, Murakami M, Hosokawa A, Uezato H (2014) Isolation of dermatophytes and related species from domestic fowl (Gallus gallus domesticus). Mycopathologia 178:135–143. https://doi.org/10.1007/s11046-014-9758-0
Zhan P, Dukiki K, Li D, Sun J, Stielow JB, van den Ende BG, Brankovics B, Menken SBJ, Mei H, Bao W, Lv G, Liu W, de Hoog GS (2018) Phylogeny of dermatophytes with genomic character evaluation of clinically distinct Trichophyton rubrum and T. violaceum. Stud Mycol 89:153–175. https://doi.org/10.1016/j.simyco.2018.02.004
Zhang ZY, Han YF, Chen WH, Liang ZQ (2019) Phylogeny and taxonomy of three new Ctenomyces (Arthrodermataceae, Onygenales) species from China. Mycokeys 47:1–16. https://doi.org/10.3897/mycokeys.47.30740
Zhang D, Gao FL, Jakovlić I, Zou H, Zhang J, Li WX, Wang GT (2020) PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour 20:348–355. https://doi.org/10.1101/489088
Zhang ZF, Zhou SY, Eurwilaichitr L, Ingsriswang S, Raza M, Chen Q, Zhao P, Liu F, Cai L (2021) Culturable mycobiota from karst caves in China II, with descriptions of 33 new species. Fungal Divers 106:29–136. https://doi.org/10.1007/s13225-020-00453-7
Zhang Z, Chen W, Liang J, Zhang L, Han Y, Huang J, Liang Z (2022) Revealing the non-overlapping characteristics between original centers and genetic diversity of Purpureocillium lilacinum. Fungal Ecol 60:101179. https://doi.org/10.1016/j.funeco.2022.101179
Zhao RL, Zhou JL, Chen J, Margaritescu S, Sánchez-Ramírez S, Hyde KD, Callac P, Parra LA, Li GJ, Moncalvo J-M (2016) Towards standardizing taxonomic ranks using divergence times—a case study for reconstruction of the Agaricus taxonomic system. Fungal Divers 78:239–292. https://doi.org/10.1007/s13225-016-0357-x
Funding
This work was supported by Key Areas of Research and Development Program of Guangdong Province (No. 2018B020205003), “Hundred” Talent Projects of Guizhou Province (Qian Ke He [2020] 6005), the National Natural Science Foundation of China (No. 32060011, 31860002) and Construction Program of Biology First-class Discipline in Guizhou (GNYL [2017] 009).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Conceptualization: Y-FH and Z-QL; data curation: ZY-Z and Y-LR; formal analysis: Z-YZ and XL; funding acquisition: Y-FH, W-HC and J-ZH; writing-original draft: Z-YZ; writing-review and editing: Z-YZ, Y-LR, XL, W-HC, J-DL, Y-FH and Z-QL. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, ZY., Ren, YL., Li, X. et al. New taxonomic framework for Arthrodermataceae: a comprehensive analysis based on their phylogenetic reconstruction, divergence time estimation, phylogenetic split network, and phylogeography. Antonie van Leeuwenhoek 115, 1319–1333 (2022). https://doi.org/10.1007/s10482-022-01774-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-022-01774-0