Abstract
Entomophthoroid fungi represent an ecologically important group of fungal pathogens on insects. Here, the whole mitogenome of Conidiobolus heterosporus, one of the entomophthoroid fungi, was described and compared to those early branching fungi with available mitogenomes. The 53,364-bp circular mitogenome of C. heterosporus contained two rRNA genes, 14 standard protein-coding genes, 26 tRNA genes, and three free-standing ORFs. Thirty introns interrupted nine mitochondrial genes. Phylogenetic analysis based on mitochondrion-encoded proteins revealed that C. heterosporus was most close to Zancudomyces culisetae in the Zoopagomycota of basal fungi. Comparison on mitogenomes of 23 basal fungi revealed great variabilities in terms of mitogenome conformation (circular or linear), genetic code (codes 1, 4, or 16), AT contents (53.3–85.5%), etc. These mitogenomes varied from 12.0 to 97.3 kb in sizes, mainly due to different numbers of genes and introns. They showed frequent DNA rearrangement events and a high variability of gene order, although high synteny and conserved gene order were also present between closely related species. By reporting the first mitogenome in Entomophthoromycotina and the second in Zoopagomycota, this study greatly enhanced our understanding on evolution of basal fungi.
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Alnakeeb K, Petersen TN, Sicheritzpontén T (2017) Norgal: extraction and de novo assembly of mitochondrial DNA from whole-genome sequencing data. BMC Bioinf 18(1):510–517. https://doi.org/10.1186/s12859-017-1927-y
Batko A (1964) Notes on entomophthoraceous fungi in Poland. Entomophaga. Men Hors Ser 2:129–131
Ben-Ze’ev I, Kenneth RG (1982a) Features-criteria of taxonomic value in the Entomophthorales: I. A revision of the Batkoan classification. Mycotaxon 14:393–455
Ben-Ze’ev I, Kenneth RG (1982b) Features-criteria of taxonomic value in the Entomophthorales: II. A revision of the genus Erynia Nowakowski 1881 (=Zoophthora Batko 1964). Mycotaxon 14:456–475
Brefeld O (1871) Untersunchngen über die Entwicklung der Empusa muscae und Empusa radicans etc. Abh naturf Ges Halle 12:1–50
Bullerwell CE, Forget L, Lang BF (2003) Evolution of monoblepharidalean fungi based on complete mitochondrial genome sequences. Nucleic Acids Res 31(6):1614–1623. https://doi.org/10.1093/nar/gkg264
Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5(6):e11147. https://doi.org/10.1371/journal.pone.0011147
Drechsler C (1953) Two new species of Conidiobolus occurring in leaf mold. Am J Bot 40(3):104–115. https://doi.org/10.1002/j.1537-2197.1953.tb06458.x
Forget L, Ustinova J, Wang Z, Huss VA, Lang BF (2002) Hyaloraphidium curvatum: a linear mitochondrial genome, tRNA editing, and an evolutionary link to lower fungi. Mol Biol Evol 19(3):310–319. https://doi.org/10.1093/oxfordjournals.molbev.a004084
Fresenius G (1858) Ueber die Pilzgattung Entomophthora. Abh Senckenberg Naturf Ges 2:201–210
Gryganskyi AP, Humber RA, Smith ME, Miadlikovska J, Wu S, Voigt K, Walther G, Anishchenko IM, Vilgalys R (2012) Molecular phylogeny of the Entomophthoromycota. Mol Phylogenet Evol 65(2):682–694. https://doi.org/10.1016/j.ympev.2012.11.001
Gryganskyi AP, Humber RA, Smith ME, Hodge K, Huang B, Voigt K, Vilgalys R (2013) Phylogenetic lineages in Entomophthoromycota. Persoonia 30:94–105. https://doi.org/10.3767/003158513X666330
Hibbett DS, Binder M, Bischo JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch HT, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Grith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüßler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547. https://doi.org/10.1016/j.mycres.2007.03.004
Huang B, Humber RA, Hodge KT (2007) A new species of Conidiobolus from Great Smoky Mountains National Park. Mycotaxon 100:227–233
Humber RA (1981) An alternative view of certain taxonomic criteria used in the Entomophthorales (Zygomycetes). Mycotaxon 13:191–240
Humber RA (1989) Synopsis of a revised classification for the Entomophthorales (Zygomycotina). Mycotaxon 36:441–460
Humber RA (2012) Entomophthoromycota: a new phylum and reclassification for entomophthoroid fungi. Mycotaxon 120:477–492. https://doi.org/10.5248/120.477
James TY, Kau F, Schoch C, Matheny PB, Hofstetter V, Cox CJ, Celio G, Geuidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MW, Grith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman A, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R ((2006a)) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822. https://doi.org/10.1038/nature05110
James TY, Letcher PM, Longcore JE, Mozley-Strandridge SE, Porter D, Powell MJ, Griffith GW, Vilgalys R (2006b) A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98:860–871. https://doi.org/10.3852/mycologia.98.6.860
James TY, Pelin A, Bonen L, Ahrendt S, Sain D, Corradi N, Stajich JE (2013) Shared signatures of parasitism and phylogenomics unite the Cryptomycota and Microsporidia. Curr Biol 23(16):1548–1553. https://doi.org/10.1016/j.cub.2013.06.057
Jones MDM, Richards TA, Hawksworth DL, David B (2011) Validation and justification of the phylum name Cryptomycota phyl. nov. IMA Fungus 2(2):173–175. https://doi.org/10.5598/imafungus.2011.02.02.08
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
Keller S (1987) Arthropod-pathogenic Entomophthorales of Switzerland. I. Conidiobolus, Entomophaga and Entomophthora. Sydowia 40:122–167
Keller S (1991) Arthropod-pathogenic Entomophthorales of Switzerland. II. Erynia, Eryniopsis, Neozygites, Zoophthora and Tarichium. Sydowia 43:39–122
Keller S (2008) The arthropod-pathogenic Entomophthorales from Switzerland – is central Europe the centre of their global species-richness? Mitt Schweiz Entomol Ges 81:39–51
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lee J, Young JPW (2009) The mitochondrial genome sequence of the arbuscular mycorrhizal fungus Glomus intraradices isolate 494 and implications for the phylogenetic placement of Glomus. New Phytol 183(1):200–211. https://doi.org/10.1111/j.1469-8137.2009.02834.x
Mendoza L, Vilela R, Voelz K, Ibrahim AS, Voigt K, Lee SC (2014) Human fungal pathogens of Mucorales and Entomophthorales. Cold Spring Harb Perspect Med 5(4):1–33. https://doi.org/10.1101/cshperspect.a019562
Nadimi M, Beaudet D, Forget L, Hijri M, Lang BF (2012) Group I intron-mediated trans-splicing in mitochondria of Gigaspora rosea and a robust phylogenetic affiliation of arbuscular mycorrhizal fungi in Mortierellales. Mol Biol Evol 29:2199–2012. https://doi.org/10.1093/molbev/mss088
Nie Y, Yu CZ, Liu XY, Huang B (2012) A new species of Conidiobolus (Ancylistaceae) from Anhui, China. Mycotaxon 120:427–435 https://doi.org/10.5248/120.427
Nie Y, Tang XX, Liu XY, Huang B (2016) Conidiobolus stilbeus, a new species with mycelial strand and two types of primary conidiophores. Mycosphere 7(6):801–809. https://doi.org/10.5943/mycosphere/7/6/11
Nie Y, Tang XX, Liu XY, Huang B (2017) A new species of Conidiobolus with chlamdosporus from Dabie Mountains, eastern China. Mycosphere 8(7):809–816. https://doi.org/10.5943/mycosphere/8/7/1
Nie Y, Qin L, Yu DS, Liu XY, Huang B (2018) Two new species of Conidiobolus occurring in Anhui, China. Mycol Prog 17(10):1203–1211. https://doi.org/10.1007/s11557-018-1436-z
Nowakowski L (1883) Entomophthoreae. Przycynek do znajomosci pasorzytnych pasorzytnych grzybkow sprawiajacych pomor. Owadow. Pamietn Wydz Akad Umiej w Krakow 8:153–183
Pelin A, Pombert JF, Salvioli A, Bonen L, Bonfante P, Corradi N (2012) The mitochondrial genome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals two unsuspected trans-splicing events of group I introns. New Phytol 194:836–845. https://doi.org/10.1111/j.1469-8137.2012.04072.x
Remaudière G, Keller S (1980) Revision systematique des generes d’Entomophthoraceae a potentialite entomopathogene. Mycotaxon 11:323–338
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574 https://doi.org/10.1093/bioinformatics/btg180
Sandor S, Zhang YJ, Xu JP (2018) Fungal mitochondrial genomes and genetic polymorphisms. Appl Microbiol Biotechnol 102:9433–9448
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108(5):1028–1046. https://doi.org/10.3852/16-042
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
Thaxter R (1888) The Entomophthoreae of the United States. Mem Boston Soc Nat Hist 4:133–201
van de Sande WW (2012) Phylogenetic analysis of the complete mitochondrial genome of Madurella mycetomatis confirms its taxonomic position within the order Sordariales. PLoS One 7(6):e38654. https://doi.org/10.1371/journal.pone.0038654
Vilela R, Silva SMS, Correa FR, Dominguez E, Mendoza L (2010) Morphologic and phylogenetic characterization of Conidiobolus lamprauges recovered from infected sheep. J Clin Microbiol 48:427–432. https://doi.org/10.1128/JCM.01589-09
Voigt K, Kirk PM (2011) Recent developments in the taxonomic affiliation and phylogenetic positioning of fungi: impact in applied microbiology and environmental biotechnology. Appl Microbiol Biotechnol 90(1):41–57. https://doi.org/10.1007/s00253-011-3143-4
Wang L, Zhang S, Li JH, Zhang YJ (2018) Mitochondrial genome, comparative analysis and evolutionary insights into the entomopathogenic fungus Hirsutella thompsonii. Environ Microbiol 20(9):3393–3405. https://doi.org/10.1111/1462-2920.14379
Watanabe M, Lee K, Goto K, Kumagai S, Sugita-Konishi Y, Hara-Kudo Y (2010) Rapid and effective DNA extraction method with bead grinding for a large amount of fungal DNA. J Food Prot 73(6):1077–1084. https://doi.org/10.4315/0362-028X-73.6.1077
Zhang S, Wang XN, Zhang XL, Liu XZ, Zhang YJ (2017a) Complete mitochondrial genome of the endophytic fungus Pestalotiopsis fici: features and evolution. Appl Microbiol Biotechnol 101(4):1593–1604. https://doi.org/10.1007/s00253-017-8112-0
Zhang YJ, Yang XQ, Zhang S, Humber RA, Xu J (2017b) Genomic analyses reveal low mitochondrial and high nuclear diversity in the cyclosporin-producing fungus Tolypocladium inflatum. Appl Microbiol Biotechnol 101(23-24):8517–8531. https://doi.org/10.1007/s00253-017-8574-0
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This work was supported by the National Natural Science Foundation of China (Grant Nos. 31272096, 31471821, 31572060, and 31872162), the Natural Science Foundation of Shanxi Province (201601D011065), and the Research Project Supported by Shanxi Scholarship Council of China (2017-015).
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Nie, Y., Wang, L., Cai, Y. et al. Mitochondrial genome of the entomophthoroid fungus Conidiobolus heterosporus provides insights into evolution of basal fungi. Appl Microbiol Biotechnol 103, 1379–1391 (2019). https://doi.org/10.1007/s00253-018-9549-5
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DOI: https://doi.org/10.1007/s00253-018-9549-5