Seven new Neocallimastigomycota genera from wild, zoo-housed, and domesticated herbivores greatly expand the taxonomic diversity of the phylum

LITERATURE CITED

• Akin D, Borneman W, Windham W. 1988. Rumen fungi: morphological types from Georgia cattle and the attack on forage cell walls. Biosystems 21:385–391.
   PubMed Web of Science ®Google Scholar
• Akin D, Lyon C, Windham W, Rigsby L. 1989. Physical degradation of lignified stem tissues by ruminal fungi. Applied and Environmental Microbiology 55:611–616.
   PubMed Web of Science ®Google Scholar
• Ariyawansa HA, Hyde KD, Jayasiri SC, Buyck B, Thilini Chethana KW, Dai DQ, Dai YC, Daranaama DA, Jayawardena RS, Lücking R, Ghobad-Nejhad M, Niskanen T, Thambugala KM, Voigt K, Zhao RL, Li G-J, Doilom M, Boonmee S, Yang, ZL, Cai Q, Cui Y-Y, Bahkali AH, Chen J, Cui BK, Chen JJ, Dayarathne MC, Dissanayake AJ, Ekanayaka AH, Hashimoto A, Hongsanan S, Jones EBG, Larsson E, Li WJ, Li Q-R, Liu JK, Luo ZL, Maharachchikumbura SSN, Mapook A, McKenzie EHC, Norphanphoun C, Konta S, Pang KL, Perera RH, Phookamsak R, Phukhamsakda C, Pinruan U, Randrianjohany E, Singtripop C, Tanaka K, Tian CM, Tibpromma S, Abdel-Wahab MA, Wanasinghe DN, Wijayawardene NN, Zhang JF, Zhang H, Abdel-Aziz FA, Wedin M, Westberg M, Ammirati JF, Bulgakov T, Lima DX, Callaghan TM, Callac P, Chang CH, Coca LF, Dal-Forno M, Dollhofer V, Fliegerová K, Greiner K, Griffith GW, Ho H-M, Hofstetter V, Jeewon R, Kang JC, Kirk PM, Kytövuori I, Lawrey JD, Xing J, Li H, Liu ZY, Liu XZ, Liimatainen K, Lumbsch HT, Matsumura M, Moncada B, Nuankaew S, Parnmen S, de Azevedo Santiago ALCM, Sommai S, de Souza CAF, de Souza-Motta CM, Su HY, Suetrong S, Wang Y, Wei S-F, Wen T-C, Yuan HS, Zhou LW, Réblová M, Fournier J, Camporesi E, Luangsa-ard JJ, Tasanathai K, Khonsanit A, Thanakitpipattana D, Somrithipol S, Diederich P, Millanes AM, Common RS, Stadler M, Yan JY, Li X, Lee HW, Nguyen TTT, Lee HB, Battistin B, Marsico O, Vizzini A, Vila J, Ercole E, Eberhardt U, Simonini G, Wen H-A, Chen X-H, Miettinen O, Spirin V, Hernawati. 2015. Fungal diversity notes 111–252: taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity 75:27– 274.
   Web of Science ®Google Scholar
• Barr D, Yanke L, Bae H, McAllister T, Cheng K. 1995. Contributions on the morphology and taxonomy of some rumen fungi from Canada. Mycotaxon 54:203–214.
   Web of Science ®Google Scholar
• Barr DJ, Kudo H, Jakober KD, Cheng KJ. 1989. Morphology and development of rumen fungi: Neocallimastix sp., Piromyces communis, and Orpinomyces bovis gen.nov., sp.nov. Canadian Journal of Botany 67 2815–2824.
   Google Scholar
• Breton A, Bernalier A, Dusser M, Fonty G, Gaillard-Martinie B, Guitlot J. 1990. Anaeromyces mucronatus nov. gen., nov. sp. A new strictly anaerobic rumen fungus with polycentric thallus. FEMS Microbiology Letters 70:177–182.
   Web of Science ®Google Scholar
• Breton A, Dusser M, Gaillard-Martine B, Guillot J, Millet L, Prensier G. 1991. Piromyces rhizinflata nov. sp., a strictly anaerobic fungus from faeces of the Saharian ass: a morphological, metabolic and ultrastructural study. FEMS Microbiology Letters 82:1–8.
   Web of Science ®Google Scholar
• Calkins S, Elledge NC, Hanafy RA, Elshahed MS, Youssef NH. 2016. A fast and reliable procedure for spore collection from anaerobic fungi: application for RNA uptake and long-term storage of isolates. Journal of Microbiological Methods 127:206–213.
   PubMed Web of Science ®Google Scholar
• Callaghan TM, Podmirseg SM, Hohlweck D, Edwards JE, Puniya AK, Dagar SS, Griffith GW. 2015. Buwchfawromyces eastonii gen. nov., sp. nov.: a new anaerobic fungus (Neocallimastigomycota) isolated from buffalo faeces. Mycokeys 9:11–28.
   Web of Science ®Google Scholar
• Couger MB, Youssef NH, Struchtemeyer CG, Liggenstoffer AS, Elshahed MS. 2015. Transcriptomic analysis of lignocellulosic biomass degradation by the anaerobic fungal isolate Orpinomyces sp. strain C1A. Biotechnology for Biofuels 8:208. Dagar SS, Kumar S, Griffith GW, Edwards JE, Callaghan TM, Singh R, Nagpal AK, Puniya AK. 2015. A new anaerobic fungus (Oontomyces anksri gen. nov., sp. nov.) from the digestive tract of the Indian camel (Camelus dromedarius). Fungal Biology 19:731–737.
   Google Scholar
• Dagar SS, Kumar S, Mudgil P, Singh R, Puniya AK. 2011. D1/D2 domain of large-subunit ribosomal DNA for differentiation of Orpinomyces spp. Applied and Environmental Microbiology 77:6722–6725.
   Google Scholar
• Gold JJ, Heath IB, Bauchop T. 1988. Ultrastructural description of a new chytrid genus of caecum anaerobe, Caecomyces equi gen. nov., sp. nov., assigned to the Neocallimasticaceae BioSystems 21:403–415.
   PubMed Web of Science ®Google Scholar
• Gruninger RJ, Puniya AK, Callaghan TM, Edwards JE, Youssef N, Dagar SS, Fliegerova K, Griffith GW, Forster R, Tsang A, McAllister T, Elshahed MS. 2014. Anaerobic fungi (phylum Neocallimastigomycota): advances in understanding of their taxonomy, life cycle, ecology, role, and biotechnological potential. FEMS Microbiology Ecology. 90:1–17.
   PubMed Web of Science ®Google Scholar
• Hanafy RA, Elshahed MS, Liggenstoffer AS, Griffith GW, Youssef NH. 2017. Pecoramyces ruminantium, gen. nov., sp. nov., an anaerobic gut fungus from the feces of cattle and sheep. Mycologia 109:231–243.
   PubMed Web of Science ®Google Scholar
• Hanafy RA, Elshahed MS, Youssef NH. 2018. Feramyces austinii, gen. nov., sp. nov., an anaerobic gut fungus from rumen and fecal samples of wild Barbary sheep and fallow deer. Mycologia 110:513–525.
   Google Scholar
• Heath BI, Bauchop T, Skipp RA. 1983. Assignment of the rumen anaerobe Neocallimastix frontalis to the Spizellomycetales (Chytridiomycetes) on the basis of its polyflagellate zoospore ultrastructure. Canadian Journal of Botany 61:295–307.
   Google Scholar
• Henske JK, Gilmore SP, Knop D, Cunningham FJ, Sexton JA, Smallwood CR, Shutthanandan V, Evans JE, Theodorou MK, O’Malley MA. 2017. Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus. Biotechnology for Biofuels 10:305–305.
   PubMed Web of Science ®Google Scholar
• Ho YW, Bar DJS, Abdullah N, Jalaludin S, Kudo H. 1993. A new species of Piromyces from the rumen of deer in Malaysia. Mycotaxon 47:285–293.
   Web of Science ®Google Scholar
• Ho YW, Barr DJS. 1995. Classification of anaerobic gut fungi from herbivores with emphasis on rumen fungi from malaysia. Mycologia 87:655–677.
   Web of Science ®Google Scholar
• Hungate RE. 1969. A roll tube method for cultivation of strict anaerobes. Methods in Microbiology 3:117–132.
   Google Scholar
• Joshi A, Lanjekar VB, Dhakephalkar PK, Callaghan TM, Griffith GW, Dagar SS. 2018. Liebetanzomyces polymorphus gen. et sp. nov., a new anaerobic fungus (Neocallimastigomycota) isolated from the rumen of a goat. Mycokeys 40:89–110.
   Web of Science ®Google Scholar
• Kittelmann S, Naylor GE, Koolaard JP, Janssen PH. 2012. A proposed taxonomy of anaerobic fungi (class Neocallimastigomycetes) suitable for large-scale sequence-based community structure analysis. PLoS ONE 7:e36866.
   PubMed Web of Science ®Google Scholar
• Kittelmann S, Seedorf H, Walters WA, Clemente JC, Knight R, Gordon JI, Janssen PH. 2013. Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS ONE 8:e47879.
   PubMed Web of Science ®Google Scholar
• Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–1874.
   PubMed Web of Science ®Google Scholar
• Li GJ, Hyde KD, Zhao RL, Hongsanan S, Abdel-Aziz FA, Abdel-Wahab MA, Alvarado P, Alves-Silva G, Ammirati JF, Ariyawansa HA, Baghela A, Bahkali AH, Beug M, Bhat DJ, Bojantchev D, Boonpratuang T, Bulgakov TS, Camporesi E, Boro MC, Ceska O, Chakraborty D, Chen JJ, Chethana KWT, Chomnunti P, Consiglio G, Cui BK, Dai DQ, Dai YC, Daranagama DA, Das K, Dayarathne MC, De Crop E, De Oliveira RJV, de Souza CAF, de Souza JI, Dentinger BTM, Dissanayake AJ, Doilom M, Drechsler-Santos ER, Ghobad-Nejhad M, Gilmore SP, Góes-Neto A, Gorczak M, Haitjema CH, Hapuarachchi KK, Hashimoto A, He MQ, Henske JK, Hirayama K, Iribarren MJ, Jayasiri SC, Jayawardena RS, Jeon SJ, Jerônimo GH, Jesus AL, Jones EBG, Kang JC, Karunarathna SC, Kirk PM, Konta S, Kuhnert E, Langer E, Lee HS, Lee HB, Li WJ, Li XH, Liimatainen K, Lima FX, Lin CG, Liu JK, Liu XZ, Liu ZY, Luangsa-ard JJ, Lücking R, Lumbsch HT, Lumyong S, Leaño EM, Marano AV, Matsumura M, McKenzie EHC, Mongkolsamrit S, Mortimer PE, Nguyen TTT, Niskanen T, Norphanphoun C, O’Malley MA, Parnmen S, Pawłowska J, Perera RH, Phookamsak R, Phukhamsakda C, Pires-Zottarelli CLA, Raspé O, Reck MA, Rocha SCO, de Santiago ALCMA, Senanayake IC, Setti L, Shang QJ, Singh SK, Sir EB, Solomon KV, Song J, Srikitikulchai P, Stadler M, Suetrong S, Takahashi H, Takahashi T, Tanaka K, Tang LP, Thambugala KM, Thanakitpipattana D, Theodorou MK, Thongbai B, Thummarukcharoen T, Tian Q, Tibpromma S, Verbeken A, Vizzini A, Vlasák J, Voigt K, Wanasinghe DN, Wang Y, Weerakoon G, Wen HA, Wen TC, Wijayawardene NN, Wongkanoun S, Wrzosek M, Xiao YP, Xu JC, Yan JY, Yang J, Da Yang S, Hu Y, Zhang JF, Zhao J, Zhou LW, Peršoh D, Phillips AJL, Maharachchikumbura SSN. 2016. Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity 78:1–237.
   Web of Science ®Google Scholar
• Li J, Health B, Bauchop T. 1990. Piromyces mae and Piromyces dumbonica, two new species of uniflagellate anaerobic chytridiomycete fungi from the hindgut of the horse and elephant. Canadian Journal of Botany 68:1021–1033.
   Google Scholar
• Liggenstoffer AS, Youssef NH, Couger MB, Elshahed MS. 2010. Phylogenetic diversity and community structure of anaerobic fungi (phylum Neocallimastigomycota) in ruminant and non-ruminant herbivores. The ISME Journal 4:1225–1235.
   PubMed Web of Science ®Google Scholar
• McSweeney CS, Denman SE, Mackie RI. 2005. Rumen bacteria. In: Makkar HPS, McSweeney CS, eds. Methods in gut microbial ecology for ruminants. Dordrecht, The Netherlands: Springer. p. 23–37.
   Google Scholar
• Mura E, Edwards J, Kittelmann S, Kaerger K, Voigt K, Mrázek J, Moniello G, Fliegerova K. 2019. Anaerobic fungal communities differ along the horse digestive tract. Fungal Biology 123:240–246.
   PubMed Web of Science ®Google Scholar
• Nagpal R, Puniya AK, Sehgal JP, Singh K. 2011. In vitro fibrolytic potential of anaerobic rumen fungi from ruminants and non-ruminant herbivores. Mycoscience 52:31–38.
   Web of Science ®Google Scholar
• Nakamura T, Yamada KD, Tomii K, Katoh K. 2018. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 34:2490–2492.
   PubMed Web of Science ®Google Scholar
• Ozkose E, Thomas BJ, Davies DR, Griffith GW, Theodorou MK. 2001. Cyllamyces aberensis gen. nov. sp.nov., a new anaerobic gut fungus with branched sporangiophores isolated from cattle. Canadian Journal of Botany 79:666–673.
   Google Scholar
• Paul SS, Bu D, Xu J, Hyde KD, Yu Z. 2018. A phylogenetic census of global diversity of gut anaerobic fungi and a new taxonomic framework. Fungal Diversity 89:253–266.
   Web of Science ®Google Scholar
• Paul SS, Deb SM, Punia BS, Singh D, Kumar R. 2010. Fibrolytic potential of anaerobic fungi (Piromyces sp.) isolated from wild cattle and blue bulls in pure culture and effect of their addition on in vitro fermentation of wheat straw and methane emission by rumen fluid of buffaloes. Journal of the Science of Food and Agriculture 90:1218–1226.
   PubMed Web of Science ®Google Scholar
• Ranganathan A, Smith OP, Youssef NH, Struchtemeyer CG, Atiyeh HK, Elshahed MS. 2017. Utilizing anaerobic fungi for two-stage sugar extraction and biofuel production from lignocellulosic biomass. Frontiers in Microbiology 8:635.
   PubMed Web of Science ®Google Scholar
• Solomon KV, Haitjema CH, Henske JK, Gilmore SP, Borges-Rivera D, Lipzen A, Brewer HM, Purvine SO, Wright AT, Theodorou MK, Grigoriev IV, Regev A, Thompson DA, O’Malley MA. 2016. Early-branching gut fungi possess a large, comprehensive array of biomass-degrading enzymes. Science 351:1192.
   PubMed Web of Science ®Google Scholar
• Tuckwell DS, Nicholson MJ, McSweeney CS, Theodorou MK, Brookman JL. 2005. The rapid assignment of ruminal fungi to presumptive genera using ITS1 and ITS2 RNA secondary structures to produce group-specific fingerprints. Microbiology 151:1557–1567.
   PubMed Web of Science ®Google Scholar
• Wang X, Liu X, Groenewald JZ. 2017. Phylogeny of anaerobic fungi (phylum Neocallimastigomycota), with contributions from yak in China. Antonie Van Leeuwenhoek 110:87–103.
   PubMed Web of Science ®Google Scholar
• Young D, Dollhofer V, Callaghan TM, Reitberger S, Lebuhn M, Benz JP. 2018. Isolation, identification and characterization of lignocellulolytic aerobic and anaerobic fungi in one- and two-phase biogas plants. Bioresoure Technology 268:470–479.
   PubMed Web of Science ®Google Scholar
• Youssef NH, Couger MB, Struchtemeyer CG, Liggenstoffer AS, Prade RA, Najar FZ, Atiyeh HK, Wilkins MR, Elshahed MS. 2013. Genome of the anaerobic fungus Orpinomyces sp. C1A reveals the unique evolutionary history of a remarkable plant biomass degrader. Applied and Environmental Microbiology 79:4620–4634.
   PubMed Web of Science ®Google Scholar