Anaerobic gut fungi: Advances in isolation, culture, and cellulolytic enzyme discovery for biofuel production

Biotechnology and Bioengineering

Volumn 111, Issue 8, 2014, Pages 1471-1482

  Haitjema, Charles H ^a   Solomon, Kevin V ^a   Henske, John K ^a   Theodorou, Michael K ^a,b   O'Malley, Michelle A ^a  

^a University of California   (United States)

^b HARPER ADAMS UNIVERSITY   (United Kingdom)

Author keywords

Anaerobic fungi; Biofuels; Cellulase; Cellulosome; Hydrogenosome

Indexed keywords

BACTERIA; BAST FIBERS; BIOFUELS; BIOMASS; MAMMALS;

ANAEROBIC FUNGUS; BIOTECHNOLOGY APPLICATIONS; CELLULASE; CELLULOSOMES; EVOLUTIONARY HISTORY; HYDROGENOSOME; LONG-TERM PRESERVATION; MOLECULAR CHARACTERIZATION;

FUNGI;

BIOFUEL; CARBOHYDRATE DERIVATIVE; CELLULASE; CELLULOSOME; LIGNOCELLULOSE; FUNGAL PROTEIN;

ANAEROBIC GUT FUNGUS; ARTICLE; BIOENERGY; BIOFUEL PRODUCTION; BIOMASS; BIOTECHNOLOGICAL PRODUCTION; BIOTRANSFORMATION; BOVIDS; DECOMPOSITION; FUNGUS; FUNGUS CULTURE; FUNGUS GROWTH; FUNGUS ISOLATION; HERBIVORE; NONHUMAN; ANIMAL; CARBOHYDRATE METABOLISM; CULTURE TECHNIQUE; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PROCEDURES;

ANIMALS; BIOFUELS; BIOMASS; CARBOHYDRATE METABOLISM; CELL CULTURE TECHNIQUES; CELLULASE; FUNGAL PROTEINS; FUNGI; GASTROINTESTINAL TRACT; INDUSTRIAL MICROBIOLOGY; RUMINANTS;

EID: 84903152521     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25264     Document Type: Article

References (97)

1. Adessi C, Matton G, Ayala G, Turcatti G, Mermod JJ, Mayer P, Kawashima E. 2000. Solid phase DNA amplification: Characterisation of primer attachment and amplification mechanisms. Nucleic Acids Res 28(20):E87.
2. Akin DE, Borneman WS, Lyon CE. 1990. Degradation of leaf blades and stems by monocentric and polycentric isolates of ruminal fungi. Anim Feed Sci Technol 31(3-4):205-221.
3. Akin DE, Lyon CE, Windham WR, Rigsby LL. 1989. Physical degradation of lignified stem tissues by ruminal fungi. Appl Environ Microbiol 55(3):611-616.
4. Akin DE, Rigsby LL. 1987. Mixed fungal populations and lignocellulosic tissue degradation in the bovine rumen. Appl Environ Microbiol 53(9):1987-1995.
5. Ali BR, Zhou L, Graves FM, Freedman RB, Black GW, Gilbert HJ, Hazelwood GP. 1995. Cellulases and hemicellulases of the anaerobic fungus Piromyces constitute a multiprotein cellulose-binding complex and are encoded by multigene families. FEMS Microbiol Lett 125(1):15-21.
6. Anderson TD, Robson SA, Jiang XW, Malmirchegini GR, Fierobe HP, Lazazzera BA, Clubb RT. 2011. Assembly of minicellulosomes on the surface of Bacillus subtilis. Appl Environ Microbiol 77(14):4849-4858.
7. Balch WE, Wolfe RS. 1976. New approach to the cultivation of methanogenic bacteria: 2-Mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressureized atmosphere. Appl Environ Microbiol 32(6):781-791.
8. Borneman WS, Akin DE, Ljungdahl LG. 1989. Fermentation products and plant cell wall-degrading enzymes produced by monocentric and polycentric anaerobic ruminal fungi. Appl Environ Microbiol 55(5):1066-1073.
9. Boxma B, Voncken F, Jannink S, van Alen T, Akhmanova A, van Weelden SW, van Hellemond JJ, Ricard G, Huynen M, Tielens AG, Hackstein JH. 2004. The anaerobic chytridiomycete fungus Piromyces sp. E2 produces ethanol via pyruvate:formate lyase and an alcohol dehydrogenase E. Mol Microbiol 51(5):1389-1399.
10. Brookman JL, Mennim G, Trinci AP, Theodorou MK, Tuckwell DS. 2000a. Identification and characterization of anaerobic gut fungi using molecular methodologies based on ribosomal ITS1 and 185 rRNA. Microbiology 146(Pt 2):393-403.
11. Brookman JL, Nicholson MJ. 2005. Anaerobic fungal populations. In: Makkar HPS, McSweeney CS, editors. Methods in gut microbial ecology for ruminants. Dordrecht, Netherlands: Springer. p 139-150.
12. Brookman JL, Ozkose E, Rogers S, Trinci AP, Theodorou MK. 2000b. Identification of spores in the polycentric anaerobic gut fungi which enhance their ability to survive. FEMS Microbiol Ecol 31(3):261-267.
13. Brownlee AG. 1988. A rapid DNA isolation procedure applicable to any refractory filamentous fungi. Fungal Genet Newsl 35:8.
14. Brownlee AG. 1989. Remarkably AT-rich genomic DNA from the anaerobic fungus Neocallimastix. Nucleic Acids Res 17(4):1327-1335.
15. Bryant MP. 1972. Commentary on the Hungate technique for culture of anaerobic bacteria. Am J Clin Nutr 25(12):1324-1328.
16. Cao YC, Yang HJ, Zhang DF. 2013. Enzymatic characteristics of crude feruloyl and acetyl esterases of rumen fungus Neocallimastix sp. YAK11 isolated from yak (Bos grunniens). J Anim Physiol Anim Nutr (Berl) 97(2):363-373.
17. Chen HL, Chen YC, Lu MY, Chang JJ, Wang HT, Ke HM, Wang TY, Ruan SK, Wang TY, Hung KY, Cho HY, Lin WT, Shih MC, Li WH. 2012a. A highly efficient beta-glucosidase from the buffalo rumen fungus Neocallimastix patriciarum W5. Biotechnol Biofuels 5(1):24.
18. Chen YC, Chiang YC, Hsu FY, Tsai LC, Cheng HL. 2012b. Structural modeling and further improvement in pH stability and activity of a highly-active xylanase from an uncultured rumen fungus. Bioresour Technol 123:125-134.
19. Chen YC, Tsai SD, Cheng HL, Chien CY, Hu CY, Cheng TY. 2007. Caecomyces sympodialis sp. nov., a new rumen fungus isolated from Bos indicus. Mycologia 99(1):125-130.
20. Cheng YF, Edwards JE, Allison GG, Zhu WY, Theodorou MK. 2009. Diversity and activity of enriched ruminal cultures of anaerobic fungi and methanogens grown together on lignocellulose in consecutive batch culture. Bioresour Technol 100(20):4821-4828.
21. Chu CY, Tseng CW, Yueh PY, Duan CH, Liu JR. 2011. Molecular cloning and characterization of a beta-glucanase from Piromyces rhizinflatus. J Biosci Bioeng 111(5):541-546.
22. Comlekcioglu U, Ozkose E, Tutus A, Akyol I, Ekinci MS. 2010. Cloning and characterization of cellulase and xylanase coding genes from anaerobic fungus Neocallimastix sp GMLF1. Int J Agric Biol 12(5):691-696.
23. Davies DR, Theodorou MK, Lawrence MI, Trinci AP. 1993. Distribution of anaerobic fungi in the digestive tract of cattle and their survival in faeces. J Gen Microbiol 139(Pt 6):1395-1400.
24. Denman SE, Nicholson MJ, Brookman JL, Theodorou MK, McSweeney CS. 2008. Detection and monitoring of anaerobic rumen fungi using an ARISA method. Lett Appl Microbiol 47(6):492-499.
25. Dijkerman R, Op den Camp HJ, Van der Drift C, Vogels GD. 1997. The role of the cellulolytic high molecular mass (HMM) complex of the anaerobic fungus Piromyces sp. strain E2 in the hydrolysis of microcrystalline cellulose. Arch Microbiol 167(2-3):137-142.
26. Dijkerman R, Vervuren MB, Op Den Camp HJ, van der Drift C. 1996. Adsorption characteristics of cellulolytic enzymes from the anaerobic fungus Piromyces sp. strain E2 on microcrystalline cellulose. Appl Environ Microbiol 62(1):20-25.
27. Dressman D, Yan H, Traverso G, Kinzler KW, Vogelstein B. 2003. Transforming single DNA molecules into fluorescent magnetic particles for detection and enumeration of genetic variations. Proc Natl Acad Sci USA 100(15):8817-8822.
28. Durand R, Rascle C, Fischer M, Fevre M. 1997. Transient expression of the beta-glucuronidase gene after biolistic transformation of the anaerobic fungus Neocallimastix frontalis. Curr Genet 31(2):158-161.
29. Fontes CM, Gilbert HJ. 2010. Cellulosomes: Highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Annu Rev Biochem 79(1):655-681.
30. France J, Dhanoa MS, Theodorou MK, Lister SJ, Davies DR, Isac D. 1993. A model to interpret gas accumulation profiles associated with in-vitro degradation of ruminant feeds. J Theor Biol 163(1):99-111.
31. Gefen G, Anbar M, Morag E, Lamed R, Bayer EA. 2012. Enhanced cellulose degradation by targeted integration of a cohesin-fused beta-glucosidase into the Clostridium thermocellum cellulosome. Proc Natl Acad Sci USA 109(26):10298-10303.
32. 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(3-4):403-415.
33. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644-652.
34. Harhangi HR, Akhmanova AS, Emmens R, van der Drift C, de Laat WT, van Dijken JP, Jetten MS, Pronk JT, Op den Camp HJ. 2003. Xylose metabolism in the anaerobic fungus Piromyces sp. strain E2 follows the bacterial pathway. Arch Microbiol 180(2):134-141.
35. Harhangi HR, Steenbakkers PJ, Akhmanova A, Jetten MS, van der Drift C, Op den Camp HJ. 2002. A highly expressed family 1 beta-glucosidase with transglycosylation capacity from the anaerobic fungus Piromyces sp. E2. Biochim Biophys Acta 1574(3):293-303.
36. Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T, Mackie RI, Pennacchio LA, Tringe SG, Visel A, Woyke T, Wang Z, Rubin EM. 2011. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331(6016):463-467.
37. Ho YW, Barr DJS. 1995. Classification of anaerobic gut fungi from herbivores with emphasis on rumen fungi from Malaysia. Mycologia 87(5):655-677.
38. Hungate RE. 1966. The rumen and its microbes. New York: Academic Press. p 533.
39. Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, Bateman A, Bernard T, Binns D, Bork P, Burge S, de Castro E, Coggill P, Corbett M, Das U, Daugherty L, Duquenne L, Finn RD, Fraser M, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, McMenamin C, Mi H, Mutowo-Muellenet P, Mulder N, Natale D, Orengo C, Pesseat S, Punta M, Quinn AF, Rivoire C, Sangrador-Vegas A, Selengut JD, Sigrist CJ, Scheremetjew M, Tate J, Thimmajanarthanan M, Thomas PD, Wu CH, Yeats C, Yong SY. 2012. InterPro in 2011: New developments in the family and domain prediction database. Nucleic Acids Res 40(Database issue):D306-D312.
40. Hungate RE, Macy J. 1973. The roll-tube method for cultivation of strict anaerobes. Bull Ecol Res Commun 17:123-126.
41. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. 2008. NCBI BLAST: A better web interface. Nucleic Acids Res 36(Web Server issue):W5-W9.
42. Keller O, Kollmar M, Stanke M, Waack S. 2011. A novel hybrid gene prediction method employing protein multiple sequence alignments. Bioinformatics 27(6):757-763.
43. Kim S, Baek SH, Lee K, Hahn JS. 2013. Cellulosic ethanol production using a yeast consortium displaying a minicellulosome and beta-glucosidase. Microb Cell Fact 12(1):14.
44. Leng N, Dawson JA, Thomson JA, Ruotti V, Rissman AI, Smits BM, Haag JD, Gould MN, Stewart RM, Kendziorski C. 2013. EBSeq: An empirical Bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics 29(8):1035-1043.
45. Li XL, Chen H, Ljungdahl LG. 1997. Two cellulases, CelA and CelC, from the polycentric anaerobic fungus Orpinomyces strain PC-2 contain N-terminal docking domains for a cellulase-hemicellulase complex. Appl Environ Microbiol 63(12):4721-4728.
46. Li B, Dewey CN. 2011. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12(1):323.
47. Liggenstoffer AS, Youssef NH, Couger MB, Elshahed MS. 2010. Phylogenetic diversity and community structure of anaerobic gut fungi (phylum Neocallimastigomycota) in ruminant and non-ruminant herbivores. ISME J 4(10):1225-1235.
48. Lockhart RJ, Van Dyke MI, Beadle IR, Humphreys P, McCarthy AJ. 2006. Molecular biological detection of anaerobic gut fungi (Neocallimastigales) from landfill sites. Appl Environ Microbiol 72(8):5659-5661.
49. Lowe SE, Theodorou MK, Trinci AP. 1987. Cellulases and xylanase of an anaerobic rumen fungus grown on wheat straw, wheat straw holocellulose, cellulose, and xylan. Appl Environ Microbiol 53(6):1216-1223.
50. Lukashin AV, Borodovsky M. 1998. GeneMark.hmm: New solutions for gene finding. Nucleic Acids Res 26(4):1107-1115.
51. Marvin-Sikkema FD, Lahpor GA, Kraak MN, Gottschal JC, Prins RA. 1992. Characterization of an anaerobic fungus from llama faeces. J Gen Microbiol 138(10):2235-2241.
52. Marvin-Sikkema FD, Pedro Gomes TM, Grivet JP, Gottschal JC, Prins RA. 1993. Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Arch Microbiol 160(5):388-396.
53. Marvin-Sikkema FD, Richardson AJ, Stewart CS, Gottschal JC, Prins RA. 1990. Influence of hydrogen-consuming bacteria on cellulose degradation by anaerobic fungi. Appl Environ Microbiol 56(12):3793-3797.
54. McDonald JE, Houghton JN, Rooks DJ, Allison HE, McCarthy AJ. 2012. The microbial ecology of anaerobic cellulose degradation in municipal waste landfill sites: Evidence of a role for fibrobacters. Environ Microbiol 14(4):1077-1087.
55. Miller TL, Wolin MJ. 1974. A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl Microbiol 27(5):985-987.
56. Müller M. 1993. Review article: The hydrogenosome. J Gen Microbiol 139(12):2879-2889.
57. Nagpal R, Puniya AK, Sehgal JP, Singh K. 2012. Survival of anaerobic fungus Caecomyces sp in various preservation methods: A comparative study. Mycoscience 53(6):427-432.
58. Nagy T, Tunnicliffe RB, Higgins LD, Walters C, Gilbert HJ, Williamson MP. 2007. Characterization of a double dockerin from the cellulosome of the anaerobic fungus Piromyces equi. J Mol Biol 373(3):612-622.
59. Nicholson MJ, Theodorou MK, Brookman JL. 2005. Molecular analysis of the anaerobic rumen fungus Orpinomyces-Insights into an AT-rich genome. Microbiology 151(Pt 1):121-133.
60. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH. 2008. Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinform Online 4:193-201.
61. Novotna Z, Prochazka J, Simunek J, Fliegerova K. 2010. Xylanases of anaerobic fungus Anaeromyces mucronatus. Folia Microbiol (Praha) 55(4):363-367.
62. O'Malley MA, Theodorou MK, Kaiser CA. 2012. Evaluating expression and catalytic activity of anaerobic fungal fibrolytic enzymes native topiromyces sp E2 in Saccharomyces cerevisiae. Environ Prog Sustain Energy 31(1):37-46.
63. Orpin CG. 1975. Studies on the rumen flagellate Neocallimastix frontalis. J Gen Microbiol 91(2):249-262.
64. Orpin CG. 1976. Studies on the rumen flagellate Sphaeromonas communis. J Gen Microbiol 94(2):270-280.
65. Orpin CG. 1977. The rumen flagellate Piromonas communis: Its life-history and invasion of plant material in the rumen. J Gen Microbiol 99(1):107-117.
66. Orpin CG. 1981. Isolation of cellulolytic phycomycete fungi from the caecum of the horse. J Gen Microbiol 123(2):287-296.
67. Orpin CG, Munn EA. 1986. Neocallimastix-Patriciarum Sp-Nov, a New Member of the Neocallimasticaceae Inhabiting the Rumen of Sheep. Transactions of the British Mycological Society 86(1):178-181.
68. Ozkose E, Thomas BJ, Davies DR, Griffith GW, Theodorou MK. 2001. Cyllamyces aberensisgen.nov. sp.nov., a new anaerobic gut fungus with branched sporangiophores isolated from cattle. Canadian Journal of Botany 79(6):666-673.
69. Raghothama S, Eberhardt RY, Simpson P, Wigelsworth D, White P, Hazlewood GP, Nagy T, Gilbert HJ, Williamson MP. 2001. Characterization of a cellulosome dockerin domain from the anaerobic fungus Piromyces equi. Nat Struct Biol 8(9):775-778.
70. Rusk N. 2009. Cheap third-generation sequencing. Nat Methods 6(4):244-244.
71. Sakurada M, Tsuzuki Y, Morgavi DP, Tomita Y, Onodera R. 1995. Simple method for cryopreservation of an anaerobic rumen fungus using ethylene glycol and rumen fluid. FEMS Microbiol Lett 127(3):171-174.
72. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW, Miller AN, Wingfield MJ, Aime MC, An KD, Bai FY, Barreto RW, Begerow D, Bergeron MJ, Blackwell M, Boekhout T, Bogale M, Boonyuen N, Burgaz AR, Buyck B, Cai L, Cai Q, Cardinali G, Chaverri P, Coppins BJ, Crespo A, Cubas P, Cummings C, Damm U, de Beer ZW, de Hoog GS, Del-Prado R, B D, Dieguez-Uribeondo J, Divakar PK, Douglas B, Duenas M, Duong TA, Eberhardt U, Edwards JE, Elshahed MS, Fliegerova K, Furtado M, Garcia MA, Ge ZW, Griffith GW, Griffiths K, Groenewald JZ, Groenewald M, Grube M, Gryzenhout M, Guo LD, Hagen F, Hambleton S, Hamelin RC, Hansen K, Harrold P, Heller G, Herrera G, Hirayama K, Hirooka Y, Ho HM, Hoffmann K, Hofstetter V, Hognabba F, Hollingsworth PM, Hong SB, Hosaka K, Houbraken J, Hughes K, Huhtinen S, Hyde KD, James T, Johnson EM, Johnson JE, Johnston PR, Jones EB, Kelly LJ, Kirk PM, Knapp DG, Koljalg U, GM K, Kurtzman CP, Landvik S, Leavitt SD, Liggenstoffer AS, Liimatainen K, Lombard L, Luangsa-Ard JJ, Lumbsch HT, Maganti H, Maharachchikumbura SS, Martin MP, May TW, McTaggart AR, Methven AS, Meyer W, Moncalvo JM, Mongkolsamrit S, Nagy LG, Nilsson RH, Niskanen T, Nyilasi I, Okada G, Okane I, Olariaga I, Otte J, Papp T, Park D, Petkovits T, Pino-Bodas R, Quaedvlieg W, Raja HA, Redecker D, T R, Ruibal C, Sarmiento-Ramirez JM, Schmitt I, Schussler A, Shearer C, Sotome K, Stefani FO, Stenroos S, Stielow B, Stockinger H, Suetrong S, Suh SO, Sung GH, Suzuki M, Tanaka K, Tedersoo L, Telleria MT, Tretter E, Untereiner WA, Urbina H, Vagvolgyi C, Vialle A, Vu TD, Walther G, Wang QM, Wang Y, Weir BS, Weiss M, White MM, Xu J, Yahr R, Yang ZL, Yurkov A, Zamora JC, Zhang N, Zhuang WY, Schindel D, Consortium FB. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109(16):6241-6246.
73. Shendure J, Ji H. 2008. Next-generation DNA sequencing. Nat Biotechnol 26(10):1135-1145.
74. Solomon KV, Haitjema CH, Thompson DA, O'Malley MA. 2014. Extracting data from the muck: Deriving biological insight from complex microbial communities and non-model organisms with next generation sequencing. Curr Opin Biotechnol 28C:103-110.
75. Somerville C. 2006. The billion-ton biofuels vision. Science 312(5778):1277.
76. Steenbakkers PJM, Freelove A, van Cranenbroek B, Sweegers BMC, Harhangi HR, Vogels GD, Hazlewood GP, Gilbert HJ, den Camp HJMO. 2002b. The major component of the cellulosomes of anaerobic fungi from the genus Piromyces is a family 48 glycoside hydrolase. DNA Sequence 13(6):313-320.
77. Steenbakkers PJ, Harhangi HR, Bosscher MW, van der Hooft MM, Keltjens JT, van der Drift C, Vogels GD, op den Camp HJ. 2003. beta-Glucosidase in cellulosome of the anaerobic fungus Piromyces sp. strain E2 is a family 3 glycoside hydrolase. Biochem J 370(Pt 3):963-970.
78. Steenbakkers PJ, Li XL, Ximenes EA, Arts JG, Chen H, Ljungdahl LG, Op Den Camp HJ. 2001. Noncatalytic docking domains of cellulosomes of anaerobic fungi. J Bacteriol 183(18):5325-5333.
79. Steenbakkers PJ, Ubhayasekera W, Goossen HJ, van Lierop EM, van der Drift C, Vogels GD, Mowbray SL, Op den Camp HJ. 2002a. An intron-containing glycoside hydrolase family 9 cellulase gene encodes the dominant 90 kDa component of the cellulosome of the anaerobic fungus Piromyces sp. strain E2. Biochem J 365(Pt 1):193-204.
80. Teunissen MJ, Smits AA, Op denCamp, Huis HJ, in 't, Veld JH, Vogels GD. 1991. Fermentation of cellulose and production of cellulolytic and xylanolytic enzymes by anaerobic fungi from ruminant and non-ruminant herbivores. Arch Microbiol 156(4):290-296.
81. Theodorou MK, Brookman J, Trinci APJ. 2005. Anaerobic fungi. In: Makkar HPS, McSweeney CS, editors. Methods in gut microbial ecology for ruminants Dordrecht: Springer Netherlands. pp. 55-66.
82. Theodorou MK, Davies DR, Nielsen BB, Lawrence MIG, Trinci APJ. 1995. Determination of growth of anaerobic fungi on soluble and cellulosic substrates using a pressure transducer. Microbiology-UK 141(3):671-678.
83. Theodorou MK, Gill M, King-Spooner C, Beever DE. 1990. Enumeration of anaerobic chytridiomycetes as thallus-forming units: novel method for quantification of fibrolytic fungal populations from the digestive tract ecosystem. Appl Environ Microbiol 56(4):1073-1078.
84. Theodorou MK, Lowe SE, Trinci APJ. 1992. Anaerobic fungi and the rumen ecosystem. In: Carrol GC, Wicklow DT, editors. The fungal community: its organization and role in the ecosystem, second edition. New York: Marcel Dekker. pp 43-72.
85. Theodorou MK, Mennim G, Davies DR, Zhu WY, Trinci APJ, Brookman JL. 1996. Anaerobic fungi in the digestive tract of mammalian herbivores and their potential for exploitation. Proc Nutr Soc 55(3):913-926.
86. Tsai KP, Calza RE. 1992. Enzyme-based DNA extraction from zoospores of ruminal fungi. Fungal Genet Newsl 39:86-88.
87. Tsai SL, DaSilva NA, Chen W. 2013. Functional display of complex cellulosomes on the yeast surface via adaptive assembly. ACS Synth Biol 2(1):14-21.
88. Tseng CW, Ko TP, Guo RT, Huang JW, Wang HC, Huang CH, Cheng YS, Wang AH, Liu JR. 2011. Substrate binding of a GH5 endoglucanase from the ruminal fungus Piromyces rhizinflata. Acta Crystallogr Sect F Struct Biol Cryst Commun 67(Pt 10):1189-1194.
89. 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.
90. van der Giezen M, Rechinger KB, Svendsen I, Durand R, Hirt RP, Fevre M, Embley TM, Prins RA. 1997. A mitochondrial-like targeting signal on the hydrogenosomal malic enzyme from the anaerobic fungus Neocallimastix frontalis: support for the hypothesis that hydrogenosomes are modified mitochondria. Mol Microbiol 23(1):11-21.
91. Wang TY, Chen HL, Lu MY, Chen YC, Sung HM, Mao CT, Cho HY, Ke HM, Hwa TY, Ruan SK, Hung KY, Chen CK, Li JY, Wu YC, Chen YH, Chou SP, Tsai YW, Chu TC, Shih CC, Li WH, Shih MC. 2011. Functional characterization of cellulases identified from the cow rumen fungus Neocallimastix patriciarum W5 by transcriptomic and secretomic analyses. Biotechnol Biofuels 4:24.
92. Wood TM, Wilson CA. 1995. Studies on the capacity of the cellulase of the anaerobic rumen fungus Piromonas communis P to degrade hydrogen bond-ordered cellulose. Appl Microbiol Biotechnol 43(3):572-578.
93. Yang HJ, Yue Q. 2012. Effect of glucose addition and N sources in defined media on fibrolytic activity profiles of Neocallimastix sp. YQ1 grown on corn stover. J Anim Physiol Anim Nutr (Berl) 96(4):554-562.
94. Yarlett N, Orpin CG, Munn EA, Yarlett NC, Greenwood CA. 1986. Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 236(3):729-739.
95. Yassour M, Pfiffner J, Levin JZ, Adiconis X, Gnirke A, Nusbaum C, Thompson DA, Friedman N, Regev A. 2010. Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species. Genome Biol 11(8):R87.
96. Youssef NH, Couger MB, Struchtemeyer CG, Liggenstoffer AS, Prade RA, Najar FZ, Atiyeh HK, Wilkins MR, Elshahed MS. 2013. The genome of the anaerobic fungus Orpinomyces sp. strain C1A reveals the unique evolutionary history of a remarkable plant biomass degrader. Appl Environ Microbiol 79(15):4620-4634.
97. Zerbino DR, Birney E. 2008. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18(5):821-829.