Abstract
Ophiocordycipitaceae is a diverse fungal family comprising multiple ecologically, economically, medicinally, and culturally important fungal species; however, only four species of the family have available mitochondrial genomes (mitogenomes). In this study, the complete mitogenome of the nematode endoparasitic fungus Hirsutella vermicola in Ophiocordycipitaceae was sequenced, and a comparative mitogenomic analysis of Ophiocordycipitaceae was performed. We found that the 53,793-bp circular mitogenome of H. vermicola, except for standard fungal mitochondrial genes, harbors seven introns acquired possibly through lateral transfer from other fungi and three free-standing open reading frames (ORFs) coding for hypothetical proteins. Phylogenetic analysis based on concatenated mitochondrial protein sequences confirmed its placement in Ophiocordycipitaceae. Comparison on five mitogenomes of Ophiocordycipitaceae revealed great variation on their sizes, from 35.2 kb in Tolypocladium ophioglossoides to 157.5 kb in Ophiocordyceps sinensis, mainly due to variable numbers of introns (from 7 to 54) as well as variable lengths of intergenic regions. The five mitogenomes, however, are highly syntenic to each other in terms of gene order, the presence of an intronic ORF encoding ribosomal protein S3 within rnl, and the nad2/nad3 joining pattern. Our study is the first report of the mitogenome of H. vermicola and has facilitated the understanding of mitogenome evolution of Ophiocordycipitaceae.
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References
Aguileta G, de Vienne DM, Ross ON, Hood ME, Giraud T, Petit E, Gabaldon T (2014) High variability of mitochondrial gene order among fungi. Genome Biol Evol 6(2):451–465
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27(2):573–580
Bushley KE, Raja R, Jaiswal P, Cumbie JS, Nonogaki M, Boyd AE, Owensby CA, Knaus BJ, Elser J, Miller D, Di Y, McPhail KL, Spatafora JW (2013) The genome of Tolypocladium inflatum: evolution, organization, and expression of the cyclosporin biosynthetic gene cluster. PLoS Genet 9(6):e1003496
Dhillion SS, Svarstad H, Amundsen C, Bugge HC (2002) Bioprospecting: effects on environment and development. Ambio 31(6):491–493
Evans HC, Elliot SL, Hughes DP (2011) Ophiocordyceps unilateralis: a keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests? Commun Integr Biol 4(5):598–602
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42(Database issue):D222–D230
Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680–682
Huang FL, Li YQ, Chen XN (2017) The complete mitochondrial genome of a medicinal fungus, Tolypocladium ophioglossoides. Mitochondr DNA Part B 2(1):95–96
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth & Bisby’s dictionary of the fungi, 10th edn. CAB International, Wallingford
Kurtz S, Schleiermacher C (1999) REPuter: fast computation of maximal repeats in complete genomes. Bioinformatics 15(5):426–427
Lai Y, Liu K, Zhang X, Zhang X, Li K, Wang N, Shu C, Wu Y, Wang C, Bushley KE, Xiang M, Liu X (2014) Comparative genomics and transcriptomics analyses reveal divergent lifestyle features of nematode endoparasitic fungus Hirsutella minnesotensis. Genome Biol Evol 6(11):3077–3093
Lanfear R, Calcott B, Ho SY, Guindon S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29(6):1695–1701
Laslett D, Canbäck B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32(1):11–16
Laslett D, Canbäck B (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24(2):172–175
Li Y, Hu X-D, Yang R-H, Hsiang T, Wang K, Liang D-Q, Liang F, Cao D-M, Zhou F, Wen G, Yao Y-J (2015) Complete mitochondrial genome of the medicinal fungus Ophiocordyceps sinensis. Sci Rep 5:13892
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25(5):955–964
Nadimi M, Daubois L, Hijri M (2016) Mitochondrial comparative genomics and phylogenetic signal assessment of mtDNA among arbuscular mycorrhizal fungi. Mol Phylogenet Evol 98:74–83
Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. Available from http://beast.bio.ed.ac.uk/Tracer
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna 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(3):539–542
Shen XY, Li T, Chen S, Fan L, Gao J, Hou CL (2015) Characterization and phylogenetic analysis of the mitochondrial genome of Shiraia bambusicola reveals special features in the order of Pleosporales. PLoS One 10(3):e0116466
Simmons DR, Kepler RM, Rehner SA, Groden E (2015) Phylogeny of Hirsutella species (Ophiocordycipitaceae) from the USA: remedying the paucity of Hirsutella sequence data. IMA Fungus 6(2):345–356
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313
Summerbell RC, Gueidan C, Schroers H-J, de Hoog GS, Starink M, Rosete YA, Guarro J, Scott JA (2011) Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium. Stud Mycol 68(1):139–162
Sun J, Park SY, Kang S, Liu X, Qiu J, Xiang M (2015) Development of a transformation system for Hirsutella spp. and visualization of the mode of nematode infection by GFP-labeled H. minnesotensis. Sci Rep 5(5):29–44
Sung G-H, Hywel-Jones NL, Sung J-M, Luangsa-ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57(1):5–59
Sung GH, Poinar GO Jr, Spatafora JW (2008) The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal–arthropod symbioses. Mol Phylogenet Evol 49(2):495–502
Wang N, Zhang Y, Hussain M, Li K, Xiang M, Liu X (2016) The mitochondrial genome of the nematode endoparasitic fungus Hirsutella rhossiliensis. Mitochondr DNA Part B 1(1):114–115
Xiang MC, Yang EC, Xiao QM, Liu XZ, Chen SY, Xiang MC, Xiao QM, Chen SY (2006) Hirsutella vermicola sp. nov., a new species parasitizing bacteria-feeding nematodes. Fungal Divers 22(4):255–265
Zhang YJ, Zhang S, Liu XZ, Wen HA, Wang M (2010) A simple method of genomic DNA extraction suitable for analysis of bulk fungal strains. Lett Appl Microbiol 51(1):114–118
Zhang YJ, Li EW, Wang CS, Li YL, Liu XZ (2012) Ophiocordyceps sinensis, the flagship fungus of China: terminology, life strategy and ecology. Mycology 3(1):2–10
Zhang YJ, Zhang S, Zhang GZ, Liu XZ, Wang CS, Xu JP (2015) Comparison of mitochondrial genomes provides insights into intron dynamics and evolution in the caterpillar fungus Cordyceps militaris. Fungal Genet Biol 77:95–107
Zhang YJ, Zhang S, Liu X (2016) The complete mitochondrial genome of the nematode endoparasitic fungus Hirsutella minnesotensis. Mitochondr DNA Part A 27(4):2693–2694
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
Zhang YJ, Zhao YX, Zhang S, Chen L, Liu XZ (2017b) Reanalysis of the mitochondrial genome of the pneumocandin-producing fungus Glarea lozoyensis. Acta Microbiol Sin. doi:10.13343/j.cnki.wsxb.20160416
Zou ZW, Min Q, Cheng SY, Xin TR, Xia B (2017) The complete mitochondrial genome of Thitarodes sejilaensis (Lepidoptera: Hepialidae), a host insect of Ophiocordyceps sinensis and its implication in taxonomic revision of Hepialus adopted in China. Gene 601:44–55
Acknowledgements
This study was funded by the National Science Foundation of China (81102759), the Natural Science Foundation of Shanxi Province (2014021030-2, 201601D011065), the Fund Program for the Scientific Activities of Selected Returned Overseas Professionals in Shanxi Province, and the Special Fund for Large Scientific Instruments and Equipments in Shanxi Province.
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Zhang, YJ., Zhang, HY., Liu, XZ. et al. Mitochondrial genome of the nematode endoparasitic fungus Hirsutella vermicola reveals a high level of synteny in the family Ophiocordycipitaceae . Appl Microbiol Biotechnol 101, 3295–3304 (2017). https://doi.org/10.1007/s00253-017-8257-x
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DOI: https://doi.org/10.1007/s00253-017-8257-x