Abstract
Gongronella is a genus of fungi in Mucorales (Mucoromycota). Some of its members have important biotechnological applications, but until now, not a single mitogenome has been characterized in Gongronella. Here, we present the complete mitogenome assembly of Gongronella sp. w5, a soil isolate known to interact with plants and several fungi. Its 36,593-bp circular mitogenome encodes the large and small subunit rRNAs, 14 standard mitochondrial proteins, 24 tRNAs, three free-standing ORF proteins, and the RNA subunit of RNase P (rnpB). These genes arrange in an order novel to known fungal mitogenomes. Three group I introns are present in the cob, cox1, and nad5 genes, respectively, and they are probably acquired by horizontal gene transfer. Phylogenetic analysis based on mitochondrion-encoded proteins supports the grouping of Gongronella sp. w5 with Absidia glauca, forming the Cunninghamellaceae clade within Mucoromycota. Gongronella and most other Mucoromycota species are predicted to use the standard genetic code in mitochondrial translation, rather than code 4 assigned by GenBank. A comparison among seven publicly available mitogenomes in Mucoromycota reveals the presence of the same 14 typical protein-coding genes plus rnpB, yet substantial variation in mitogenome size, intron number, gene order, and orientation. In this comparison, the uniqueness of Gongronella is evident from similarly large differences to its closest phylogenetic neighbor, A. glauca. This study promotes our understanding of fungal evolution in Mucoromycota.
Key points
• This study reports the first mitogenome in Gongronella, which presents a novel gene order.
• Different Mucoromycota mitogenomes show substantial variation of gene organizations.
• Most Mucoromycota species use the standard genetic code to translate mitochondrial genes.
Similar content being viewed by others
Data availability
The mitogenome sequence of Gongronella sp. w5 is available in GenBank under accession number OK572620.
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
Cannon P, Aguirre-Hudson B, Aime MC, Ainsworth AM, Bidartondo MI, Gaya E, Hawksworth D, Kirk P, Leitch IJ, Lücking R (2018) Definition and diversity. In: Willis KJ (ed) State of the world’s fungi 2018. report. Royal Botanic Gardens, Kew, pp 4–11
Chatre L, Ricchetti M (2014) Are mitochondria the Achilles’ heel of the kingdom Fungi? Curr Opin Microbiol 20:49–54
Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5(6):e11147
Dierckxsens N, Mardulyn P, Smits G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45(4):e18
Doilom M, Guo J-W, Phookamsak R, Mortimer PE, Karunarathna SC, Dong W, Liao C-F, Yan K, Pem D, Suwannarach N, Promputtha I, Lumyong S, Xu J-C (2020) Screening of phosphate-solubilizing fungi from air and soil in Yunnan, China: four novel species in Aspergillus, Gongronella, Penicillium, and Talaromyces. Front Microbiol 11:585215
Dong Y, Sun Q, Zhang Y, Wang X, Liu P, Xiao Y, Fang Z (2018) Complete genome of Gongronella sp. w5 provides insight into its relationship with plant. J Biotechnol 286:1–4
Dujon B (2020) Mitochondrial genetics revisited. Yeast 37(2):191–205
Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7(10):e1002195
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797
Ehrlich R, Davyt M, Lopez I, Chalar C, Marin M (2021) On the track of the missing tRNA genes: a source of non-canonical functions? Front Mol Biosci 8:643701
Ellenberger S, Burmester A, Wöstemeyer J (2018) The fate of mitochondria after infection of the mucoralean fungus Absidia glauca by the fusion parasite Parasitella parasitica: comparison of mitochondrial genomes in zygomycetes. Mitochondr DNA A 29(1):113–120
Fan W-W, Zhang S, Zhang Y-J (2019) The complete mitochondrial genome of the Chan-hua fungus Isaria cicadae: a tale of intron evolution in Cordycipitaceae. Environ Microbiol 21(2):864–879
Fan L, Wu D, Goremykin V, Xiao J, Xu Y, Garg S, Zhang C, Martin WF, Zhu R (2020) Phylogenetic analyses with systematic taxon sampling show that mitochondria branch within Alphaproteobacteria. Nat Ecol Evol 4(9):1213–1219
Fang W, Song R, Zhang X, Zhang X, Zhang X, Wang X, Fang Z, Xiao Y (2014) Characterization of a novel β-glucosidase from Gongronella sp W5 and its application in the hydrolysis of soybean isoflavone glycosides. J Agric Food Chem 62(48):11688–11695
Gray MW (2012) Mitochondrial evolution. Cold Spring Harb Perspect Biol 4(9):a011403
Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283(5407):1476–1481
Gray MW, Burger G, Lang BF (2001) The origin and early evolution of mitochondria. Genome Biol 2(6):reviews1018.1-1018.5
Greiner S, Lehwark P, Bock R (2019) OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res 47(W1):W59–W64
Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 2.2 to 3.8 million species. Microbiol Spectr 5(4):FUNK-0052-2016
Hibbett DS, Binder M, Bischoff 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 Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, 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 Y-J, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111(5):509–547
Hu J, Zhang Y, Xu Y, Sun Q, Liu J, Fang W, Xiao Y, Kües U, Fang Z (2019) Gongronella sp. w5 elevates Coprinopsis cinerea laccase production by carbon source syntrophism and secondary metabolite induction. Appl Microbiol Biotechnol 103(1):411–425
James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan 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 MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, 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 (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443(7113):818–822
James TY, Stajich JE, Hittinger CT, Rokas A (2020) Toward a fully resolved fungal tree of life. Annu Rev Microbiol 74(1):291–313
Jin J-J, Yu W-B, Yang J-B, Song Y, Yi T-S, Li D-Z (2020) GetOrganelle: a simple and fast pipeline for de novo assembly of a complete circular chloroplast genome using genome skimming data. Genome Biol 21:241
Karnkowska A, Vacek V, Zubáčová Z, Treitli SC, Petrželková R, Eme L, Novák L, Žárský V, Barlow LD, Herman EK, Soukal P, Hroudová M, Doležal P, Stairs CW, Roger AJ, Eliáš M, Dacks JB, Vlček Č, Hampl V (2016) A eukaryote without a mitochondrial organelle. Curr Biol 26(10):1274–1284
Kazantsev AV, Rambo RP, Karimpour S, Santalucia JJR, Tainer JA, Pace NR (2011) Solution structure of RNase P RNA. RNA 17(6):1159–1171
Korovesi AG, Ntertilis M, Kouvelis VN (2018) Mt-rps3 is an ancient gene which provides insight into the evolution of fungal mitochondrial genomes. Mol Phylogenet Evol 127:74–86
Kouvelis VN, Sialakouma A, Typas MA (2008) Mitochondrial gene sequences alone or combined with ITS region sequences provide firm molecular criteria for the classification of Lecanicillium species. Mycol Res 112(7):829–844
Laforest MJ, Roewer I, Lang BF (1997) Mitochondrial tRNAs in the lower fungus Spizellomyces punctatus tRNA editing and UAG ‘Stop’ codons recognized as leucine. Nucleic Acids Res 25(3):626–632
Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34(3):772–773
Lang BF, O’Kelly C, Nerad T, Gray MW, Burger G (2002) The closest unicellular relatives of animals. Curr Biol 12(20):1773–1778
Lang BF, Lavrov D, Beck N, Steinberg SV (2012) Mitochondrial tRNA structure, identity, and evolution of the genetic code. In: Bullerwell CE (ed) Organelle genetics. Springer, Berlin, Heidelberg, Germany, pp 431–474
Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25(17):2286–2288
Liu Y, Steenkamp ET, Brinkmann H, Forget L, Philippe H, Lang BF (2009) Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evol Biol 9:272
Liu J, Peng C, Han Q, Wang M, Zhou G, Ye B, Xiao Y, Fang Z, Kües U, Druzhinina IS (2022) Coprinopsis cinerea uses laccase Lcc9 as a defense strategy to eliminate oxidative stress during fungal-fungal interactions. Appl Environl Microb 88(1):e01760-e1821
Martins MR, Santos C, Soares C, Santos C, Lima N (2020) Gongronella eborensis sp. nov., from vineyard soil of Alentejo (Portugal). Int J Syst Evol Micr 70(5):3475–3482
Molitor C, Inthavong B, Sage L, Geremia RA, Mouhamadou B (2010) Potentiality of the cox1 gene in the taxonomic resolution of soil fungi. FEMS Microbiol Lett 302(1):76–84
Moriya J, Yokogawa T (1994) A novel modified nucleoside found at the first position of the anticodon of methionine tRNA from bovine liver mitochondria. Biochemistry 33:2234–2239
Nawrocki EP, Eddy SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29(22):2933–2935
Nguyen L-T, 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(1):268–274
Nie Y, Wang L, Cai Y, Tao W, Zhang Y-J, Huang B (2019) Mitochondrial genome of the entomophthoroid fungus Conidiobolus heterosporus provides insights into evolution of basal fungi. Appl Microbiol Biotechnol 103(9):1379–1391
Pan K, Zhao N, Yin Q, Zhang T, Xu X, Fang W, Hong Y, Fang Z, Xiao Y (2014) Induction of a laccase Lcc9 from Coprinopsis cinerea by fungal coculture and its application on indigo dye decolorization. Bioresour Technol 162:45–52
Ren L-Y, Zhang S, Zhang Y-J (2021) Comparative mitogenomics of fungal species in Stachybotryaceae provides evolutionary insights into Hypocreales. Int J Mol Sci 22(24):13341
Rodríguez-Ezpeleta N, Brinkmann H, Roure B, Lartillot N, Lang BF, Philippe H (2007) Detecting and overcoming systematic errors in genome-scale phylogenies. Syst Biol 56(3):389–399
Rosario Martins M, Pereira P, Lima N, Cruz-Morais J (2013) Degradation of metalaxyl and folpet by filamentous fungi isolated from Portuguese (Alentejo) vineyard soils. Arch Environ Con Tox 65(1):67–77
Seif ER, Forget L, Martin NC, Lang BF (2003) Mitochondrial RNase P RNAs in ascomycete fungi: lineage-specific variations in RNA secondary structure. RNA 9(9):1073–1083
Seif E, Leigh J, Liu Y, Roewer I, Forget L, Lang BF (2005) Comparative mitochondrial genomics in zygomycetes: bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms. Nucleic Acids Res 33(2):734–744
Shiflett AM, Johnson PJ (2010) Mitochondrion-related organelles in eukaryotic protists. Annu Rev Microbiol 64:409–429
Siegel RW, Banta AB, Haas ES, Brown JW, Pace NR (1996) Mycoplasma fermentans simplifies our view of the catalytic core of ribonuclease P RNA. RNA 2(5):452–462
Silva de Freitas LW, Vilela de Oliveira RJ, Leite Cordeiro TR, Thuong Thuong Thi N, Lim HJ, Lee HB, Monteiro C, de Azevedo Santiago AL (2021) Gongronella pedratalhadensis, a new species of Mucorales (Mucoromycota) isolated from the Brazilian Atlantic Forest, with an identification key for the genus. Sydowia 73:61–68
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
Spatafora JW, Aime MC, Grigoriev IV, Martin F, Stajich JE, Blackwell M (2017) The fungal tree of life: from molecular systematics to genome-scale phylogenies. Microbiol Spectr 5(5):FUNK-0053-2016
Tedersoo L, Sánchez-Ramírez S, Kõljalg U, Bahram M, Döring M, Schigel D, May T, Ryberg M, Abarenkov K (2018) High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Divers 90(1):135–159
Turmel M, Bélanger A-S, Otis C, Lemieux C (2020) Complete mitogenomes of the chlorophycean green algae Bulbochaete rectangularis var. hiloensis (Oedogoniales) and Stigeoclonium helveticum (Chaetophorales) provide insight into the sequence of events that led to the acquisition of a reduced-derived pattern of evolution in the Chlamydomonadales and Sphaeropleales. Mitochondr DNA B 5(1):611–613
Vaughn JC, Mason MT, Sper-Whitis GL, Kuhlman P, Palmer JD (1995) Fungal origin by horizontal transfer of a plant mitochondrial group I intron in the chimeric coxI gene of Peperomia. J Mol Evol 41(5):563–572
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
Voigt K, James TY, Kirk PM, Santiago A, Waldman B, Griffith GW, Fu M, Radek R, Strassert JFH, Wurzbacher C, Jeronimo GH, Simmons DR, Seto K, Gentekaki E, Hurdeal VG, Hyde KD, Nguyen TTT, Lee HB (2021) Early-diverging fungal phyla: taxonomy, species concept, ecology, distribution, anthropogenic impact, and novel phylogenetic proposals. Fungal Divers 109:59–98
Wang L, Zhang S, Li J-H, Zhang Y-J (2018) Mitochondrial genome, comparative analysis and evolutionary insights into the entomopathogenic fungus Hirsutella thompsonii. Environ Microbiol 20(9):3393–3405
Wang X, Fang J, Liu P, Liu J, Fang W, Fang Z, Xiao Y (2021) Mucoromycotina fungi possess the ability to utilize plant sucrose as a carbon source: evidence from Gongronella sp. w5. Front Microbiol 11:591697
Wei F, Hong Y, Liu J, Yuan J, Fang W, Peng H, Xiao Y (2010) Gongronella sp. induces overproduction of laccase in Panus rudis. J Basic Microbiol 50(1):98–103
Wijayawardene NN, Hyde KD, Al-Ani LKT, Tedersoo L, Haelewaters D, Rajeshkumar KC, Zhao RL, Aptroot A, Leontyev DV, Saxena RK, Tokarev YS, Dai DQ, Letcher PM, Stephenson SL, Ertz D, Lumbsch HT, Kukwa M, Issi IV, Madrid H, Phillips AJL, Selbmann L, Pfliegler WP, Horvath E, Bensch K, Kirk PM, Kolarikova K, Raja HA, Radek R, Papp V, Dima B, Ma J, Malosso E, Takamatsu S, Rambold G, Gannibal PB, Triebel D, Gautam AK, Avasthi S, Suetrong S, Timdal E, Fryar SC, Delgado G, Reblova M, Doilom M, Dolatabadi S, Pawlowska JZ, Humber RA, Kodsueb R, SanchezCastro I, Goto BT, Silva DKA, de Souza FA, Oehl FR, da Silva GA, Silva IR, Blaszkowski J, Jobim K, Maia LC, Barbosa FR, Fiuza PO, Divakar PK, Shenoy BD, Castaneda-Ruiz RF, Somrithipol S, Lateef AA, Karunarathna SC, Tibpromma S, Mortimer PE, Wanasinghe DN, Phookamsak R, Xu J, Wang Y, Tian F, Alvarado P, Li DW, Kusan I, Matocec N, Mesic A, Tkalcec Z, Maharachchikumbura SSN, Papizadeh M, Heredia G, Wartchow F, Bakhshi M, Boehm E, Youssef N, Hustad VP, Lawrey JD, Santiago ALCMA, Bezerra JDP, Souza-Motta CM, Firmino AL, Tian Q, Houbraken J, Hongsanan S, Tanaka K, Dissanayake AJ, Monteiro JS, Grossart HP, Suija A, Weerakoon G, Etayo J, Tsurykau A, Vazquez V, Mungai P, Damm U, Li QR, Zhang H, Boonmee S, Lu YZ, Becerra AG, Kendrick B, Brearley FQ, Motiejunaite J, Sharma B, Khare R, Gaikwad S, Wijesundara DSA, Tang LZ, He MQ, Flakus A, Rodriguez-Flakus P, Zhurbenko MP, McKenzie EHC, Stadler M, Bhat DJ, Liu JK, Raza M, Jeewon R, Nassonova ES, Prieto M, Jayalal RGU, Erdogdu M, Yurkov A, Schnittler M, Shchepin ON, Novozhilov YK, Silva-Filho AGS, Gentekaki E, Liu P, Cavender JC, Kang Y, Mohammad S, Zhang LF, Xu RF, Li YM, Dayarathne MC, Ekanayaka AH, Wen TC, Deng CY, Pereira OL, Navathe S, Hawksworth DL, Fan XL, Dissanayake LS, Kuhnert E, Thines M (2020) Outline of Fungi and fungus-like taxa. Mycosphere 11(1):1060–1456
Zhang S, Zhang Y-J (2019) Proposal of a new nomenclature for introns in protein-coding genes in fungal mitogenomes. IMA Fungus 10:15
Zhang Y-J, Zhang S, Zhang G, Liu X, Wang C, Xu J (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 S, Wang X-N, Zhang X-L, Liu X-Z, Zhang Y-J (2017) Complete mitochondrial genome of the endophytic fungus Pestalotiopsis fici: features and evolution. Appl Microbiol Biotechnol 101(4):1593–1604
Zhang S, Bai X, Ren L-Y, Sun H-H, Tang H-P, Vaario L-M, Xu J, Zhang Y-J (2021) Dynamic evolution of eukaryotic mitochondrial and nuclear genomes: a case study in the gourmet pine mushroom Tricholoma matsutake. Environ Microbiol 23(11):7214–7230
Zhou W, Yuan H, Wang J, Yao J (2008) Production, purification and characterization of chitosanase produced by Gongronella sp. JG Lett Appl Microbiol 46(1):49–54
Zhou G, Peng C, Liu X, Chang F, Xiao Y, Liu J, Fang Z (2020) Identification and immobilization of an invertase with high specific activity and sucrose tolerance ability of Gongronella sp. w5 for high fructose syrup preparation. Front Microbiol 11:633
Acknowledgements
We thank the High Performance Simulation Platform of Shanxi University for providing computing resource.
Funding
This study was funded by the National Natural Science Foundation of China (31872162) and NSERC Canada (BFL).
Author information
Authors and Affiliations
Contributions
S.Z. and Y.J.Z. designed the research; S.W., B.F.L., Z.F., and Y.J.Z. performed the research and analyzed the data; S.Z., S.W., and Z.F. prepared the original draft of the manuscript; B.F.L. and Y.J.Z. revised and edited the final manuscript. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Ethics approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare no competing interests.
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
About this article
Cite this article
Zhang, S., Wang, S., Fang, Z. et al. Characterization of the mitogenome of Gongronella sp. w5 reveals substantial variation in Mucoromycota. Appl Microbiol Biotechnol 106, 2587–2601 (2022). https://doi.org/10.1007/s00253-022-11880-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-022-11880-8