한국미생물·생명공학회지 (Microbiology and Biotechnology Letters)

  • 제46권3호
  • /
  • Pages.300-312
  • /
  • 2018
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  • 1598-642X(pISSN)
  • /
  • 2234-7305(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
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Genome Sequencing and Genome-Wide Identification of Carbohydrate-Active Enzymes (CAZymes) in the White Rot Fungus Flammulina fennae

  • Lee, Chang-Soo (Department of Biomedical Chemistry, Research Institute for Biomedical & Health Science, College of Biomedical and Health Science, Konkuk University) ;
  • Kong, Won-Sik (Mushroom Research Division, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Park, Young-Jin (Department of Biomedical Chemistry, Research Institute for Biomedical & Health Science, College of Biomedical and Health Science, Konkuk University)
  • 투고 : 2018.08.21
  • 심사 : 2018.08.30
  • 발행 : 2018.09.28
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초록

Whole-genome sequencing of the wood-rotting fungus, Flammulina fennae, was carried out to identify carbohydrate-active enzymes (CAZymes). De novo genome assembly (31 kmer) of short reads by next-generation sequencing revealed a total genome length of 32,423,623 base pairs (39% GC). A total of 11,591 gene models in the assembled genome sequence of F. fennae were predicted by ab initio gene prediction using the AUGUSTUS tool. In a genome-wide comparison, 6,715 orthologous groups shared at least one gene with F. fennae and 10,667 (92%) of 11,591 genes for F. fennae proteins had orthologs among the Dikarya. Additionally, F. fennae contained 23 species-specific genes, of which 16 were paralogous. CAZyme identification and annotation revealed 513 CAZymes, including 82 auxiliary activities, 220 glycoside hydrolases, 85 glycosyltransferases, 20 polysaccharide lyases, 57 carbohydrate esterases, and 45 carbohydrate binding-modules in the F. fennae genome. The genome information of F. fennae increases the understanding of this basidiomycete fungus. CAZyme gene information will be useful for detailed studies of lignocellulosic biomass degradation for biotechnological and industrial applications.

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참고문헌

  1. Bas C. 1983. Flammulina in western Europe. Persoonia-Molecular Phylogeny and Evolution of Fungi 12: 51-66.
  2. Ripkova S, Hughes K, Adamcik S, Kucera V, Adamcikova K. 2010. The delimitation of Flammulina fennae. Mycol. Prog. 9: 469-484. https://doi.org/10.1007/s11557-009-0654-9
  3. Perez-Butron JL, Ferdnandez-Vicente J. 2007. Una nuevaespecie de Flammulina P. Karsten, F. cephalariae (Agaricales) encontradaen Espana. Rev. Catalana. Micol. 29: 81-91.
  4. Eriksson K, Blanchette RA, Ander P. 1990. Morphological aspects of wood degradation by fungi and bacteria. pp. 1-87. In Microbial and enzymatic degradation of wood and wood components. Springer: Berlin, Heidelberg.
  5. Rytioja J, Hildén K, Yuzon J, Hatakka A, de Vries RP, Makela MR. 2014. Plant-polysaccharide-degrading enzymes from basidiomycetes. Microbiol. Mol. Biol. Rev. 78: 614-649. https://doi.org/10.1128/MMBR.00035-14
  6. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. 2004. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382: 769-781. https://doi.org/10.1042/BJ20040892
  7. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42: D490-D495. https://doi.org/10.1093/nar/gkt1178
  8. Shoseyov O, Shani Z, Levy I. 2006. Carbohydrate binding modules: biochemical properties and novel applications. Microbiol. Mol. Biol. Rev. 70: 283-295. https://doi.org/10.1128/MMBR.00028-05
  9. Zhao Z, Liu H, Wang C, Xu JR. 2013. Correction: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 14: 274. https://doi.org/10.1186/1471-2164-14-274
  10. Park YJ, Baek JH, Lee S, Kim C, Rhee H, Kim H, et al. 2014. Whole genome and global gene expression analyses of the model mushroom Flammulina velutipes reveal a high capacity for lignocellulose degradation. PLoS One 9: e93560. https://doi.org/10.1371/journal.pone.0093560
  11. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120. https://doi.org/10.1093/bioinformatics/btu170
  12. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18: 821-829. https://doi.org/10.1101/gr.074492.107
  13. Stanke M, Morgenstern B. 2005. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 33: W465-W467. https://doi.org/10.1093/nar/gki458
  14. Buchfink B, Xie C, Huson D. 2015. Fast and sensitive protein alignment using DIAMOND, Nat. Methods 12: 59-60. https://doi.org/10.1038/nmeth.3176
  15. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, et al. 2016. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44: D279-D285. https://doi.org/10.1093/nar/gkv1344
  16. Lowe TM, Eddy SR. 1997. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964. https://doi.org/10.1093/nar/25.5.955
  17. Emms D, Kelly S. 2015. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16: 157. https://doi.org/10.1186/s13059-015-0721-2
  18. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, et al. 2005. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105-1115. https://doi.org/10.1038/nature04341
  19. Staats M, van Kan JA. 2012. Genome update of Botrytis cinerea strains B05. 10 and T4. Eukaryot. Cell 11: 1413-1414. https://doi.org/10.1128/EC.00164-12
  20. Morin E, Kohler A, Baker AR, Foulongne-Oriol M, Lombard V, Nagye LG, et al. 2012. Genome sequence of the button mushroom Agaricusbisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc. Natl. Acad. Sci. USA 109: 17501-17506. https://doi.org/10.1073/pnas.1206847109
  21. Stajich JE, Wilke SK, Ahrén D, Au CH, Birren BW, Borodovsky M, et al. 2010. Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc. Natl. Acad. Sci. USA 107: 11889-11894. https://doi.org/10.1073/pnas.1003391107
  22. Zheng P, Xia Y, Xiao G, Xiong C, Hu X, Zhang S, et al. 2011. Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol. 12: R116. https://doi.org/10.1186/gb-2011-12-11-r116
  23. Janbon G, Ormerod KL, Paulet D, Byrnes III EJ, Yadav V, Chatterjee G, et al. 2014. Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet. 10: e1004261. https://doi.org/10.1371/journal.pgen.1004261
  24. Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ, Duchaussoy F, et al. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88-92. https://doi.org/10.1038/nature06556
  25. Chen L, Gong Y, Cai Y, Liu W, Zhou Y, Xiao Y, et al. 2016. Genome sequence of the edible cultivated mushroom Lentinula edodes (Shiitake) reveals insights into lignocellulose degradation. PLoS One 11: e0160336. https://doi.org/10.1371/journal.pone.0160336
  26. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, et al. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868. https://doi.org/10.1038/nature01554
  27. Martinez D, Larrondo LF, Putnam N, Sollewijn Gelpke MD, Huang K, Chapman J, et al. 2004. Genome sequence of the lignocellu- lose degrading fungus Phanerochaete chrysosporium strain RP78. Nat. Biotechnol. 22: 695-700. https://doi.org/10.1038/nbt967
  28. Fisk DG, Ball CA, Dolinski K, Engel SR, Hong EL, Issel‐Tarver L, et al. 2006. Saccharomyces cerevisiae S288C genome annotation: a working hypothesis. Yeast 23: 857-865. https://doi.org/10.1002/yea.1400
  29. Ohm RA, De Jong JF, Lugones LG, Aerts A, Kothe E, Stajich JE, et al. 2010. Genome sequence of the model mushroom Schizophyllum commune. Nat. Biotechnol. 28: 957-963. https://doi.org/10.1038/nbt.1643
  30. Li WC, Huang CH, Chen CL, Chuang YC, Tung SY, Wang TF. 2017. Trichoderma reesei complete genome sequence, repeat-induced point mutation, and partitioning of CAZyme gene clusters. Biotechnol. Biofuels 10: 170. https://doi.org/10.1186/s13068-017-0825-x
  31. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101. https://doi.org/10.1038/nature05248
  32. Yin Y, Mao X, Yang JC, Chen X, Mao F, Xu Y. 2012. dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 40: W445-W451. https://doi.org/10.1093/nar/gks479
  33. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8: 785-786. https://doi.org/10.1038/nmeth.1701
  34. Breton C, Snajdrova L, Jeanneau C, Koca J, Imberty A. 2006. Structures and mechanisms of glycosyltransferases. Glycobiology 16: 29R-37R. https://doi.org/10.1093/glycob/cwj016
  35. Lairson LL, Henrissat B, Davies GJ, Withers SG. 2008. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77: 521-555. https://doi.org/10.1146/annurev.biochem.76.061005.092322
  36. Paulson JC, Weinstein J, Ujita EL, Riggs KJ, Lai H. 1987. The membrane-binding domain of a rat liver Golgi sialyltransferase. Biochem. Soc. Trans. 15: 618-620. https://doi.org/10.1042/bst0150618
  37. Wickner WT, Lodish HF. 1985. Multiple mechanisms of protein insertion into and across membranes. Science 230: 400-407. https://doi.org/10.1126/science.4048938
  38. Chou MM, Kendall DA. 1990. Polymeric sequences reveal a functional interrelationship between hydrophobicity and length of signal peptides. J. Biol. Chem. 265: 2873-2880,
  39. IngMarie N, Whitley P, von Heijne G. 1994. The COOH-terminal ends of internal signal and signal-anchor sequences are positioned differently in the ER translocase. J. Cell Biol. 126: 1127- 1132. https://doi.org/10.1083/jcb.126.5.1127
  40. Coutinho PM, Deleury E, Davies GJ, Henrissat B. 2003. An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328: 307-317. https://doi.org/10.1016/S0022-2836(03)00307-3
  41. Campbell JA, Davies GJ, Bulone V, Henrissat B. 1997. A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem. J. 326: 929-939. https://doi.org/10.1042/bj3260929u
  42. Mukai Y, Hirokawa T, Tomii K, Asai K, Akiyama Y, Suwa M. 2008. Identification of glycosyltransferases focusing on Golgi trans- membrane region, Trends Glycosci. Glycotechnol. 19: 41-47.
  43. Berlemont R, Martiny AC. 2016. Glycoside hydrolases across environmental microbial communities. PLoS Comput. Biol. 12: e1005300. https://doi.org/10.1371/journal.pcbi.1005300
  44. Henrissat B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280: 309-316. https://doi.org/10.1042/bj2800309
  45. Hahn M, Olsen O, Politz O, Borriss R, Heinemann U. 1995. Crystal structure and site-directed mutagenesis of Bacillus macerans endo-1,3-1,4-beta-glucanase. J. Biol. Chem. 270: 3081-3088. https://doi.org/10.1074/jbc.270.7.3081
  46. Masuda S, Endo K, Koizumi N, Hayami T, Fukazawa T, Yatsunami R, et al. 2006. Molecular identification of a novel beta-1,3-glucanase from alkaliphilic Nocardiopsis sp. strain F96. Extremophiles 10: 251-255. https://doi.org/10.1007/s00792-006-0514-3
  47. Kotake T, Hirata N, Degi Y, Ishiguro M, Kitazawa K, Takata R, et al. 2011. Endo-${\beta}$-1,3-galactanase from winter mushroom Flammulina velutipes. J. Biol. Chem. 286: 27848-27854. https://doi.org/10.1074/jbc.M111.251736
  48. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, et al. 2007. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35: W585-W587. https://doi.org/10.1093/nar/gkm259
  49. Wilson DB. 2011. Microbial diversity of cellulose hydrolysis. Curr. Opin. Microbiol. 14: 259-263. https://doi.org/10.1016/j.mib.2011.04.004
  50. Berlemont R. 2017. Distribution and diversity of enzymes for polysaccharide degradation in fungi. Sci. Rep. 7: 222. https://doi.org/10.1038/s41598-017-00258-w
  51. Eichlerova I, Homolka L, Zifcakova L, Lisa L, Dobiasova P, Baldrian P. 2015. Enzymatic systems involved in decomposition reflects the ecology and taxonomy of saprotrophic fungi. Fungal Ecol. 13: 10-22. https://doi.org/10.1016/j.funeco.2014.08.002
  52. Treseder KK, Lennon JT. 2015. Fungal traits that drive ecosystem dynamics on land. Microbiol. Mol. Biol. Rev. 79: 243-262. https://doi.org/10.1128/MMBR.00001-15
  53. Sutherland IW. 1995. Polysaccharide lyases. FEMS Microbiol. Rev. 16: 323-347. https://doi.org/10.1111/j.1574-6976.1995.tb00179.x
  54. Yip VL, Withers SG. 2006. Breakdown of oligosaccharides by the process of elimination. Curr. Opin. Chem. Biol. 10: 147-155. https://doi.org/10.1016/j.cbpa.2006.02.005
  55. Garron ML, Cygler M. 2010. Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology 20: 1547-1573. https://doi.org/10.1093/glycob/cwq122
  56. van den Brink J, de Vries RP. 2011. Fungal enzyme sets for plant polysaccharide degradation. Appl. Microbiol. Biotechnol. 91: 1477-1492. https://doi.org/10.1007/s00253-011-3473-2
  57. Xavier-Santos S, Carvalho CC, Bonfá M, Silva R, Capelari M, Gomes E. 2004. Screening for pectinolytic activity of wood-rotting basidiomycetes and characterization of the enzymes. Folia Microbiol. (Praha) 49: 46-52. https://doi.org/10.1007/BF02931645
  58. The CAZypedia Consortium. 2018. Ten years of CAZypedia: a living encyclopedia of carbohydrate-active enzymes. Glycobiology 28: 3-8. https://doi.org/10.1093/glycob/cwx089
  59. Fernandez-Fueyo E, Ruiz-Duenas FJ, Ferreira P, Floudas D, Hibbett DS, Canessa P, et al. 2012. Comparative genomics of Ceriporiopsis- subvermispora and Phanerochaetechrysosporium provide insight into selective ligninolysis. Proc. Natl. Acad. Sci. USA 109: 5458- 5463. https://doi.org/10.1073/pnas.1119912109
  60. Varnai A, Mäkelä MR, Djajadi DT, Rahikainen J, Hatakka A, Viikari L. 2014. Carbohydrate-binding modules of fungal cellulases: occurrence in nature, function, and relevance in industrial biomass conversion. Adv. Appl. Microbiol. 88: 103-165.
  61. Bornscheuer UT. 2002. Microbial carboxyl esterases: Classification, properties and application in biocatalysis. FEMS Microbiol. Rev. 26: 73-81. https://doi.org/10.1111/j.1574-6976.2002.tb00599.x
  62. Jaeger KE, Eggert T. 2002. Lipases for biotechnology. Curr. Opin. Biotechnol. 13: 390-397. https://doi.org/10.1016/S0958-1669(02)00341-5
  63. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37: D233-D238. https://doi.org/10.1093/nar/gkn663
  64. Biely P. 2012. Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnol. Adv. 30: 1575-1588. https://doi.org/10.1016/j.biotechadv.2012.04.010
  65. Adesioye FA, Makhalanyane TP, Biely P, Cowan DA. 2016. Phylogeny, classification and metagenomic bioprospecting of microbial acetyl xylanesterases. Enzyme Microb. Technol. 93: 79-91.
  66. Christov LP, Prior BA. 1993. Esterases of xylan-degrading microorganisms: Production, properties, and significance. Enzyme Microb. Technol. 15: 460-475. https://doi.org/10.1016/0141-0229(93)90078-G
  67. Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B. 2013. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol. Biofuels 6: 41. https://doi.org/10.1186/1754-6834-6-41
  68. Reiss R, Ihssen J, Richter M, Eichhorn E, Schilling B, Thony-Meyer L. 2013. Laccase versus laccase-like multi-copper oxidase: a comparative study of similar enzymes with diverse substrate spectra. PLoS One 8: e65633. https://doi.org/10.1371/journal.pone.0065633
  69. Fernandez IS, Ruiz-Duenas FJ, Santillana E, Ferreira P, Martinez MJ, Martinez AT, et al. 2009. Novel structural features in the GMC family of oxidoreductases revealed by the crystal structure of fungal aryl-alcohol oxidase. Acta Crystallogr. D65: 1196-1205.
  70. Varela E, Martinet MJ, Martinez AT. 2000. Arylalcohol oxidase pro- tein sequence: a comparison with glucose oxidase and other FAD oxidoreductases. Biochem. Biophys. Acta Protein Struct. Mol. Enzymol. 1481: 202-208. https://doi.org/10.1016/S0167-4838(00)00127-8
  71. Wierenga RK, Drenth J, Schulz GE. 1983. Comparison of the 3-dimensional protein and nucleotide structure of the FAD-binding domain of parahydroxybenzoate hydroxylase with the FAD- binding as well as NADPH-binding domains of glutathionereductase. J. Mol. Biol. 167: 725-739. https://doi.org/10.1016/S0022-2836(83)80106-5
  72. Ruiz-Duenas FJ, Martinez AT. 2009. Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb. Biotechnol. 2: 164-177. https://doi.org/10.1111/j.1751-7915.2008.00078.x
  73. Martinez AT, Ruiz-Duenas FJ, Martinez MJ, Del Rio JC, Gutierrez A. 2009. Enzymatic delignification of plant cell wall: from nature to mill. Curr. Opin. Biotechnol. 20: 348-357. https://doi.org/10.1016/j.copbio.2009.05.002
  74. Guillen F, Martinez MJ, Gutierrez A, Del Rio JC. 2005. Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int. Microbiol. 8: 195-204.
  75. Leonowicz A, Matuszewska A, Luterek J, Ziegenhagen D, Wojtas-Wasilewska M, Cho, NS, et al. 1999. Biodegradation of lignin by white rot fungi. Fungal Genet. Biol. 27: 175-185. https://doi.org/10.1006/fgbi.1999.1150

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