Mycobiology

The Korean Society of Mycology (한국균학회)
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Genome-Wide Comparison of Carbohydrate-Active Enzymes (CAZymes) Repertoire of Flammulina ononidis

  • Park, Young-Jin (Department of Integrated Biosciences, 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)
  • Received : 2018.07.16
  • Accepted : 2018.10.12
  • Published : 2018.12.31
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Abstract

Whole-genome sequencing of Flammulina ononidis, a wood-rotting basidiomycete, was performed to identify genes associated with carbohydrate-active enzymes (CAZymes). A total of 12,586 gene structures with an average length of 2009 bp were predicted by the AUGUSTUS tool from a total 35,524,258 bp length of de novo genome assembly (49.76% GC). Orthologous analysis with other fungal species revealed that 7051 groups contained at least one F. ononidis gene. In addition, 11,252 (89.5%) of 12,586 genes for F. ononidis proteins had orthologs among the Dikarya, and F. ononidis contained 8 species-specific genes, of which 5 genes were paralogous. CAZyme prediction revealed 524 CAZyme genes, including 228 for glycoside hydrolases, 21 for polysaccharide lyases, 87 for glycosyltransferases, 61 for carbohydrate esterases, 87 with auxiliary activities, and 40 for carbohydrate-binding modules in the F. ononidis genome. This genome information including CAZyme repertoire will be useful to understand lignocellulolytic machinery of this white rot fungus F. ononidis.

Keywords

References

  1. Arnolds E. Einige Pilze eines Halbtrockenrasen bei Detmold (Westfalen). Westfal Pilzbriefe. 1977;11:29-39.
  2. Ripkova S, Adamcik S, Kucera V. Flammulina ononidis - a new species for Slovakia. Czech Mycol. 2008;60:221-230. https://doi.org/10.33585/cmy.60206
  3. Łuszczynski J, Łuszczynska B, Tomaszewska A. Flammulina ononidis - first record in Poland. Acta Mycol. 2014;49:79-85. https://doi.org/10.5586/am.2014.007
  4. Ripkova S, Hughes K, Adamcik S, et al. The delimitation of Flammulina fennae. Mycol Progress. 2010;9:469-484. https://doi.org/10.1007/s11557-009-0654-9
  5. Hughes KW, McGhee LL, Methven AS, et al. Patterns of geographic speciation in the genus Flammulina based on sequences of the ribosomal ITS1-5.8S-ITS2 area. Mycologia. 1999;91:978-986. https://doi.org/10.1080/00275514.1999.12061107
  6. Psurtseva NV. Culture of Flammulina velutipes (Fr.) P.Karst. (biology and economic importance. Mikol. i Fitopatol. l987;21:477-486.
  7. Klan J, Baudisova D. Cultural, enzyme and genetic studies in the genus Flammulina Karst. Mycotaxon. 1992;43:341-350.
  8. Nobles MJ. Identification of cultures of wood inhabiting Hymenomycetes. Can J Bot. 1965;26:281-413.
  9. Marr CD. Laccase and peroxidase oxidation of spot test reagents. Mycotaxon. 1979;9:244-276.
  10. Alekhina I, Psurtseva N, Yli-Mattila T. Isozyme analysis of LE(BIN) Collection Flammulina strains. Karstenia. 2001;41:55-63. https://doi.org/10.29203/ka.2001.379
  11. Psurtseva NY, Mnoukhina AY. Morphological, physiological and enzyme variability of Flammulina P. Karst. cultures. Mikol i Fitopatol. 1998;32:49-54.
  12. Perez-Butron JL, Ferdnandez-Vicente J. Una nueva especie de Flammulina P. Karsten, F. cephalariae (Agaricales) encontrada en Espa-na. Rev Catalana Micol. 2007;29:81-91.
  13. Eriksson K, Blanchette RA, Ander P. Microbial and enzymatic degradation of wood and wood components. Berlin, Germany: Springer-Verlag; 1990.
  14. Rytioja J, Hilden K, Yuzon J, et al. Plant-polysaccharide-degrading enzymes from basidiomycetes. Microbiol Mol Biol Rev. 2014;78:614-649. https://doi.org/10.1128/MMBR.00035-14
  15. Lombard V, Golaconda Ramulu H, Drula E, et al. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490-D495. https://doi.org/10.1093/nar/gkt1178
  16. Park YJ, Baek JH, Lee S, et al. Whole genome and global gene expression analyses of the model mushroom Flammulina velutipes reveal a high capacity for lignocellulose degradation. PLoS One. 2014;9:e93560. https://doi.org/10.1371/journal.pone.0093560
  17. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114-2120. https://doi.org/10.1093/bioinformatics/btu170
  18. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18:821-829. https://doi.org/10.1101/gr.074492.107
  19. Stanke M, Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 2005;33:W465-W467. https://doi.org/10.1093/nar/gki458
  20. Buchfink B, Xie C, Huson D. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59-60. https://doi.org/10.1038/nmeth.3176
  21. Finn RD, Coggill P, Eberhardt R, et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44:D279-D285. https://doi.org/10.1093/nar/gkv1344
  22. Emms D, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16:157. https://doi.org/10.1186/s13059-015-0721-2
  23. Galagan JE, Calvo SE, Cuomo C, et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature. 2005;438:1105-1115. https://doi.org/10.1038/nature04341
  24. Staats M, van Kan JA. Genome update of Botrytis cinerea strains B05.10 and T4. Eukaryot Cell. 2012;11:1413-1414. https://doi.org/10.1128/EC.00164-12
  25. Morin E, Kohler A, Baker AR, et al. Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc Natl Acad Sci USA. 2012;109:17501-17506. https://doi.org/10.1073/pnas.1206847109
  26. Stajich JE, Wilke SK, Ahren D, et al. Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci USA. 2010;107:11889-11894. https://doi.org/10.1073/pnas.1003391107
  27. Zheng P, Xia Y, Xiao G, et al. Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol. 2011;12:R116. https://doi.org/10.1186/gb-2011-12-11-r116
  28. Janbon G, Ormerod K, Paulet D, et al. Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLOS Genet. 2014;10:e1004261. https://doi.org/10.1371/journal.pgen.1004261
  29. Martin F, Aerts A, Ahren D, et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008;452:88-92. https://doi.org/10.1038/nature06556
  30. Chen L, Gong Y, Cai Y, et al. Genome sequence of the edible cultivated mushroom Lentinula edodes (Shiitake) reveals insights into lignocellulose degradation. PloS One. 2016;11:e0160336. https://doi.org/10.1371/journal.pone.0160336
  31. Galagan JE, Calvo SE, Borkovich KA, et al. The genome sequence of the filamentous fungus Neurospora crassa. Nature. 2003;422:859-868. https://doi.org/10.1038/nature01554
  32. Martinez D, Larrondo LF, Putnam N, et al. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol. 2004;22:695-700. https://doi.org/10.1038/nbt967
  33. Fisk DG, Ball CA, Dolinski K, et al. Saccharomyces cerevisiae S288C genome annotation: a working hypothesis. Yeast. 2006;23:857-865. https://doi.org/10.1002/yea.1400
  34. Ohm RA, De Jong JF, Lugones L, et al. Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol. 2010;28:957-963. https://doi.org/10.1038/nbt.1643
  35. Li WC, Huang CH, Chen CL, et al. Trichoderma reesei complete genome sequence, repeat-induced point mutation, and partitioning of CAZyme gene clusters. Biotechnol Biofuels. 2017;10:170. https://doi.org/10.1186/s13068-017-0825-x
  36. Kamper J, Kahmann R, Bolker M, et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature. 2006;444:97-101. https://doi.org/10.1038/nature05248
  37. Yin Y, Mao X, Yang JC, et al. dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2012;40:W445-W451. https://doi.org/10.1093/nar/gks479
  38. Breton C, Snajdrova L, Jeanneau C, et al. Structures and mechanisms of glycosyltransferases. Glycobiology. 2006;16:29R-37R. https://doi.org/10.1093/glycob/cwj016
  39. Lairson LL, Henrissat B, Davies GJ, et al. Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem. 2008;77:521-555. https://doi.org/10.1146/annurev.biochem.76.061005.092322
  40. Coutinho PM, Deleury E, Davies GJ, et al. An evolving hierarchical family classification for glycosyltransferases. J Mol Biol. 2003;328:307-317. https://doi.org/10.1016/S0022-2836(03)00307-3
  41. Campbell JA, Davies GJ, Bulone V, et al. A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem J. 1997;326:929-939. https://doi.org/10.1042/bj3260929u
  42. Mukai Y, Hirokawa T, Tomii K, et al. Identification of glycosyltransferases focusing on Golgi transmembrane region. Tigg. 2007;19:41-47. https://doi.org/10.4052/tigg.19.41
  43. Berlemont R, Martiny AC. Glycoside hydrolases across environmental microbial communities. PLoS Comput Biol. 2016;12:e1005300. https://doi.org/10.1371/journal.pcbi.1005300
  44. Henrissat B. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1991;280:309-316. https://doi.org/10.1042/bj2800309
  45. Hahn M, Olsen O, Politz O, et al. Crystal structure and site-directed mutagenesis of Bacillus macerans endo-1,3-1,4-beta-glucanase. J Biol Chem. 1995;270:3081-3088. https://doi.org/10.1074/jbc.270.7.3081
  46. Masuda S, Endo K, Koizumi N, et al. Molecular identification of a novel beta-1,3-glucanase from alkaliphilic Nocardiopsis sp. strain F96. Extremophiles. 2006;10:251-255. https://doi.org/10.1007/s00792-006-0514-3
  47. Kotake T, Hirata N, Degi Y, et al. Endo-beta-1,3-galactanase from winter mushroom Flammulina velutipes. J Biol Chem. 2011;286:27848-27854. https://doi.org/10.1074/jbc.M111.251736
  48. Berlemont R. Distribution and diversity of enzymes for polysaccharide degradation in fungi. Sci Rep. 2017;7:222. https://doi.org/10.1038/s41598-017-00258-w
  49. Sutherland IW. Polysaccharide lyases. FEMS Microbiol Rev. 1995;16:323-347. https://doi.org/10.1111/j.1574-6976.1995.tb00179.x
  50. Yip VL, Withers SG. Breakdown of oligosaccharides by the process of elimination. Curr Opin Chem Biol. 2006;10:147-155. https://doi.org/10.1016/j.cbpa.2006.02.005
  51. van den Brink J, de Vries RP. Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol. 2011;91:1477-1492. https://doi.org/10.1007/s00253-011-3473-2
  52. Garron ML, Cygler M. Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology. 2010;20:1547-1573. https://doi.org/10.1093/glycob/cwq122
  53. Linhardt RJ, Galliher PM, Cooney CL. Polysaccharide lyases. Appl Biochem Biotechnol. 1986;12:135-176.
  54. Xavier-Santos S, Carvalho CC, Bonfa M, et al. Screening for pectinolytic activity of wood-rotting basidiomycetes and characterization of the enzymes. Folia Microbiol. 2004;49:46-52. https://doi.org/10.1007/BF02931645
  55. Boraston AB, Bolam DN, Gilbert HJ, et al. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J. 2004;382:769-781. https://doi.org/10.1042/BJ20040892
  56. Shoseyov O, Shani Z, Levy I. Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev. 2006;70:283-295. https://doi.org/10.1128/MMBR.00028-05
  57. Varnai A, Makela MR, Djajadi DT, et al. Carbohydrate-binding modules of fungal cellulases: occurrence in nature, function, and relevance in industrial biomass conversion. Adv Appl Microbiol. 2014;88:103-165.
  58. Bornscheuer UT. Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol Rev. 2002;26:73-81. https://doi.org/10.1111/j.1574-6976.2002.tb00599.x
  59. Jaeger KE, Eggert T. Lipases for biotechnology. Curr Opin Biotechnol. 2002;13:390-397. https://doi.org/10.1016/S0958-1669(02)00341-5
  60. Cantarel BL, Coutinho PM, Rancurel C, et al. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 2009;37:D233-D238. https://doi.org/10.1093/nar/gkn663
  61. Biely P. Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnol Adv. 2012;30:1575-1588. https://doi.org/10.1016/j.biotechadv.2012.04.010
  62. Adesioye FA, Makhalanyane TP, Biely P, et al. Phylogeny, classification and metagenomic bioprospecting of microbial acetyl xylan esterases. Enzyme Microb Technol. 2016;93-94:79-91. https://doi.org/10.1016/j.enzmictec.2016.07.001
  63. Wei Y, Schottel JL, Derewenda U, et al. A novel variant of the catalytic triad in the Streptomyces scabies esterase. Nat Struct Biol. 1995;2:218-223. https://doi.org/10.1038/nsb0395-218
  64. Petersen EI, Valinger G, Solkner B, et al. A novel esterase from Burkholderia gladioli which shows high deacetylation activity on cephalosporins is related to beta-lactamases and DD-peptidases. J Biotechnol. 2001;89:11-25. https://doi.org/10.1016/S0168-1656(01)00284-X
  65. Christov LP, Prior BA. Esterases of xylan-degrading microorganisms: production, properties, and significance. Enzyme Microb Technol. 1993;15:460-475. https://doi.org/10.1016/0141-0229(93)90078-G
  66. Levasseur A, Drula E, Lombard V, et al. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels. 2013;6:41. https://doi.org/10.1186/1754-6834-6-41
  67. Reiss R, Ihssen J, Richter M, et al. Laccase versus laccase-like multi-copper oxidase: a comparative study of similar enzymes with diverse substrate spectra. PloS One. 2013;8:e65633. https://doi.org/10.1371/journal.pone.0065633
  68. Fernandez IS, Ruiz-Duenas FJ, Santillana E, et al. Novel structural features in the GMC family of oxidoreductases revealed by the crystal structure of fungal aryl-alcohol oxidase. Acta Crystallogr D Biol Crystallogr. 2009;65:1196-1205. https://doi.org/10.1107/S0907444909035860
  69. Varela E, Jesus Martinez M, Martinez AT, Arylalcohol oxidase protein sequence: a comparison with glucose oxidase and other FAD oxidoreductases. Biochem Biophys Acta Protein Struct Mol Enzymol. 2000;1481:202-208. https://doi.org/10.1016/S0167-4838(00)00127-8
  70. Wierenga RK, Drenth J, Schulz GE, et al. 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. 1983;167:725-739. https://doi.org/10.1016/S0022-2836(83)80106-5
  71. Fernandez-Fueyo E, Ruiz-Duenas FJ, Ferreira P, et al. Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc Natl Acad Sci USA. 2012;109:5458-5463. https://doi.org/10.1073/pnas.1119912109
  72. Martinez AT, Ruiz-Due-nas FJ, Martinez MJ, et al. Enzymatic delignification of plant cell wall: from nature to mill. Curr Opin Biotechnol. 2009;20:348-357. https://doi.org/10.1016/j.copbio.2009.05.002
  73. Ruiz-Due-nas FJ, Martinez AT. Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol. 2009;2:164-177. https://doi.org/10.1111/j.1751-7915.2008.00078.x
  74. Henrissat B, Claeyssens M, Tomme P, et al. Cellulase families revealed by hydrophobic cluster analysis. Gene. 1989;81:83-95. https://doi.org/10.1016/0378-1119(89)90339-9
  75. The CAZypedia Consortium. Ten years of CAZypedia: a living encyclopedia of carbohydrateactive enzymes. Glycobiology. 2018;28:3-8. https://doi.org/10.1093/glycob/cwx089
  76. Berlemont R, Martiny AC. Phylogenetic distribution of potential cellulases in bacteria. Appl Environ Microbiol. 2013;79:1545-1554. https://doi.org/10.1128/AEM.03305-12
  77. Berlemont R, Martiny AC. Genomic potential for polysaccharides deconstruction in bacteria. Appl Environ Microbiol. 2015;81:1513-1519. https://doi.org/10.1128/AEM.03718-14
  78. Talamantes D, Biabini N, Dang H, et al. Natural diversity of cellulases, xylanases, and chitinases in bacteria. Biotechnol Biofuels. 2016;9:133. https://doi.org/10.1186/s13068-016-0538-6
  79. Eichlerova I, Homolka L, Zifcakova L, et al. Enzymatic systems involved in decomposition reflects the ecology and taxonomy of saprotrophic fungi. Fungal Ecol. 2015;13:10-22. https://doi.org/10.1016/j.funeco.2014.08.002
  80. Treseder KK, Lennon JT. Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev. 2015;79:243-262. https://doi.org/10.1128/MMBR.00001-15
  81. Zhao Z, Liu H, Wang C, et al. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics. 2013;14:274. https://doi.org/10.1186/1471-2164-14-274

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