Classification of fungal and bacterial lytic polysaccharide monooxygenases

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Busk, Peter K ^a   Lange, Lene ^a  

^a AALBORG UNIVERSITY   (Denmark)

Author keywords

Genomic annotation; Lytic polysaccharide monooxygenases; Peptide pattern recognition; Sequence analysis; Subfamilies

Indexed keywords

CELLULOSE; HEMICELLULOSE; LYTIC POLYSACCHARIDE MONOOXYGENASE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE; MIXED FUNCTION OXIDASE; POLYSACCHARIDE;

AMINO ACID SEQUENCE; ARTICLE; ASCOMYCETES; BACTERIAL GENOME; BACTERIUM; BASIDIOMYCETES; CHYTRIDIOMYCETES; COMPUTER MODEL; ENZYME DEGRADATION; FUNGAL GENOME; GENETIC CODE; MOLECULAR GENETICS; NONHUMAN; PEPTIDE PATTERN RECOGNITION; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; ZYGOMYCETES; ANIMAL; BIOLOGY; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; CONSERVED SEQUENCE; CYTOLOGY; FUNGUS; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION;

ASCOMYCOTA; BACTERIA (MICROORGANISMS); BASIDIOMYCOTA; FUNGI;

ANIMALS; BACTERIA; CELLULOSE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; FUNGI; MIXED FUNCTION OXYGENASES; MODELS, MOLECULAR; POLYSACCHARIDES; PROTEIN CONFORMATION;

EID: 84929166559     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1601-6     Document Type: Article

References (64)

1. Agger JW, Isaksen T, Várnai A, Vidal-Melgosa S, Willats WGT, Ludwig R, et al. Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci U S A. 2014;111:6287-92.
2. Forsberg Z, Vaaje-Kolstad G, Westereng B, Bunæs AC, Stenstrøm Y, MacKenzie A, et al. Cleavage of cellulose by a CBM33 protein. Protein Sci. 2011;20:1479-83.
3. Harris PV, Welner D, McFarland KC, Re E, Navarro Poulsen J-C, Brown K, et al. Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry. 2010;49:3305-16.
4. Langston JA, Shaghasi T, Abbate E, Xu F, Vlasenko E, Sweeney MD. Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol. 2011;77:7007-15.
5. Phillips CM, Beeson WT, Cate JH, Marletta MA. Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol. 2011;6:1399-406.
6. Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sørlie M, et al. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science. 2010;330:219-22.
7. Beeson WT, Phillips CM, Cate JH, Marletta MA. Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J Am Chem Soc. 2011;134:890-2.
8. Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen J-CN, Johansen KS, et al. Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci U S A. 2011;108:15079-84.
9. Westereng B, Ishida T, Vaaje-Kolstad G, Wu M, Eijsink VGH, Igarashi K, et al. The putative endoglucanase PcGH61D from Phanerochaete chrysosporium is a metal-dependent oxidative enzyme that cleaves cellulose. PLoS One. 2011;6:e27807.
10. Isaksen T, Westereng B, Aachmann FL, Agger JW, Kracher D, Kittl R, et al. A C4-oxidizing lytic polysaccharide monooxygenase cleaving both cellulose and cello-oligosaccharides. J Biol Chem. 2014;289:2632-42.
11. Aachmann FL, Sørlie M, Skjåk-Bræk G, Eijsink VGH, Vaaje-Kolstad G. NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions. Proc Natl Acad Sci U S A. 2012;109:18779-84.
12. Li X, Beeson 4th WT, Phillips CM, Marletta MA, Cate JHD. Structural basis for substrate targeting and catalysis by fungal polysaccharide monooxygenases. Structure. 2012;20:1051-61.
13. Wu M, Beckham GT, Larsson AM, Ishida T, Kim S, Payne CM, et al. Crystal structure and computational characterization of the lytic polysaccharide monooxygenase GH61D from the basidiomycota fungus Phanerochaete chrysosporium. J Biol Chem. 2013;288:12828-39.
14. Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels. 2013;6:41.
15. Karlsson J, Saloheimo M, Siika-Aho M, Tenkanen M, Penttilä M, Tjerneld F. Homologous expression and characterization of Cel61A (EG IV) of Trichoderma reesei. Eur J Biochem. 2001;268:6498-507.
16. Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG. Novel enzymes for the degradation of cellulose. Biotechnol Biofuels. 2012;5:45.
17. Leggio LL, Welner D, De Maria L. A structural overview of GH61 proteins - fungal cellulose degrading polysaccharide monooxygenases. Comput Struct Biotechnol J. 2012;2:e201209019.
18. Hori C, Igarashi K, Katayama A, Samejima M. Effects of xylan and starch on secretome of the basidiomycete Phanerochaete chrysosporium grown on cellulose. FEMS Microbiol Lett. 2011;321:14-23.
19. Ray A, Saykhedkar S, Ayoubi-Canaan P, Hartson SD, Prade R, Mort AJ. Phanerochaete chrysosporium produces a diverse array of extracellular enzymes when grown on sorghum. Appl Microbiol Biotechnol. 2012;93:2075-89.
20. Yakovlev I, Vaaje-Kolstad G, Hietala AM, Stefáczyk E, Solheim H, Fossdal CG. Substrate-specific transcription of the enigmatic GH61 family of the pathogenic white-rot fungus Heterobasidion irregulare during growth on lignocellulose. Appl Microbiol Biotechnol. 2012;95:979-90.
21. Forsberg Z, Røhr AK, Mekasha S, Andersson KK, Eijsink VGH, Vaaje-Kolstad G, et al. Comparative study of two chitin-active and two cellulose-active AA10-type lytic polysaccharide monooxygenases. Biochemistry. 2014;53:1647-56.
22. Forsberg Z, Mackenzie AK, Sørlie M, Røhr AK, Helland R, Arvai AS, et al. Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases. Proc Natl Acad Sci U S A. 2014;111:8446-51.
23. Hemsworth GR, Henrissat B, Davies GJ, Walton PH. Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nat Chem Biol. 2014;10:122-6.
24. Busk PK, Lange L. Function-based classification of carbohydrate-active enzymes by recognition of short, conserved peptide motifs. Appl Environ Microbiol. 2013;79:3380-91.
25. Busk PK, Lange M, Pilgaard B, Lange L. Several genes encoding enzymes with the same activity are necessary for aerobic fungal degradation of cellulose in nature. PLoS One. 2014;9:e114138.
26. Stam MR, Danchin EGJ, Rancurel C, Coutinho PM, Henrissat B. Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of alpha-amylase-related proteins. Protein Eng Des Sel. 2006;19:555-62.
27. Aspeborg H, Coutinho PM, Wang Y, Brumer 3rd H, Henrissat B. Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol. 2012;12:186.
28. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009;37(Database issue):D233-8.
29. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42(Database issue):D490-5.
30. Busk PK, Lange L. A Novel Method of Providing a Library of N-Mers or Biopolymers. 2012. [WO2012101151].
31. Hemsworth GR, Taylor EJ, Kim RQ, Gregory RC, Lewis SJ, Turkenburg JP, et al. The copper active site of CBM33 polysaccharide oxygenases. J Am Chem Soc. 2013;135:6069-77.
32. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science. 2012;336:1715-9.
33. Kuhad RC, Kuhar S, Kapoor M, Sharma KK, Singh A. Lignocellulolytic microorganisms, their enzymes and possible biotechnologies based on lignocellulolytic microorganisms and their enzymes. In Lignocellulose Biotechnology: Future Prospects. I. K. International Pvt Ltd; 2007. p. 3-22.
34. Moore-Landecker E. Fungi as saprophytes. In Fundamentals of the fungi. Prentice-Hall; New Jersey, USA. 1972. p. 291-325.
35. Riley R, Salamov AA, Brown DW, Nagy LG, Floudas D, Held BW, et al. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci USA. 2014;111:9923-9928.
36. th revised edition edition. Wallingford, Oxon, UK: CABI Publishing; 1995.
37. Glass NL, Schmoll M, Cate JHD, Coradetti S. Plant cell wall deconstruction by ascomycete fungi. Annu Rev Microbiol. 2013;67:477-98.
38. Baldo A, Monod M, Mathy A, Cambier L, Bagut ET, Defaweux V, et al. Mechanisms of skin adherence and invasion by dermatophytes. Mycoses. 2012;55:218-23.
39. Ng KP, Ngeow YF, Yew SM, Hassan H, Soo-Hoo TS, Na SL, et al. Draft genome sequence of Daldinia eschscholzii isolated from blood culture. Eukaryot Cell. 2012;11:703-4.
40. Gianoulis TA, Griffin MA, Spakowicz DJ, Dunican BF, Alpha CJ, Sboner A, et al. Genomic analysis of the hydrocarbon-producing, cellulolytic, endophytic fungus Ascocoryne sarcoides. PLoS Genet. 2012;8:e1002558.
41. Ohm RA, de Jong JF, Lugones LG, Aerts A, Kothe E, Stajich JE, et al. Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol. 2010;28:957-63.
42. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389-402.
43. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 2011;39(Database issue):D225-9.
44. Bey M, Zhou S, Poidevin L, Henrissat B, Coutinho PM, Berrin J-G, et al. Cello-oligosaccharide oxidation reveals differences between Two lytic polysaccharide monooxygenases (family GH61) from Podospora anserina. Appl Environ Microbiol. 2013;79:488-96.
45. Vu VV, Beeson WT, Phillips CM, Cate JHD, Marletta MA. Determinants of regioselective hydroxylation in the fungal polysaccharide monooxygenases. J Am Chem Soc. 2014;136:562-5.
46. Vaaje-Kolstad G, Bøhle LA, Gåseidnes S, Dalhus B, Bjørås M, Mathiesen G, et al. Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J Mol Biol. 2012;416:239-54.
47. Gudmundsson M, Kim S, Wu M, Ishida T, Momeni MH, Vaaje-Kolstad G, et al. Structural and electronic snapshots during the transition from a Cu(II) to Cu(I) metal center of a lytic polysaccharide monooxygenase by X-ray photoreduction. J Biol Chem. 2014;289:18782-92.
48. Monod M. Secreted proteases from dermatophytes. Mycopathologia. 2008;166:285-94.
49. Martinez DA, Oliver BG, Gräser Y, Goldberg JM, Li W, Martinez-Rossi NM, et al. Comparative genome analysis of Trichophyton rubrum and related dermatophytes reveals candidate genes involved in infection. MBio. 2012;3:e00259-00212.
50. Zaugg C, Monod M, Weber J, Harshman K, Pradervand S, Thomas J, et al. Gene expression profiling in the human pathogenic dermatophyte Trichophyton rubrum during growth on proteins. Eukaryot Cell. 2009;8:241-50.
51. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, et al. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science. 2005;307:1321-4.
52. Baron O, Cassaing S, Percodani J, Berry A, Linas M-D, Fabre R, et al. Nucleotide sequencing for diagnosis of sinusal infection by Schizophyllum commune, an uncommon pathogenic fungus. J Clin Microbiol. 2006;44:3042-3.
53. Tanaka H, Takizawa K, Baba O, Maeda T, Fukushima K, Shinya K, et al. Basidiomycosis: Schizophyllum commune osteomyelitis in a dog. J Vet Med Sci. 2008;70:1257-9.
54. Zugmaier W, Bauer R, Oberwinkler F. Mycoparasitism of some tremella species. Mycologia. 1994;86:49-56.
55. Fitzpatrick DA. Horizontal gene transfer in fungi. FEMS Microbiol Lett. 2012;329:1-8.
56. Jumpponen A, Jones KL. Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol. 2010;186:496-513.
57. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol. 2010;12:2885-93.
58. Spring J. Major transitions in evolution by genome fusions: from prokaryotes to eukaryotes, metazoans, bilaterians and vertebrates. J Struct Funct Genomics. 2003;3:19-25.
59. Richardson M. The ecology of the Zygomycetes and its impact on environmental exposure. Clin Microbiol Infect. 2009;15 Suppl 5:2-9.
60. Busk PK, Lange L. Cellulolytic potential of thermophilic species from four fungal orders. AMB Express. 2013;3:47.
61. Busk PK. The meaning of life - On cactus finches, evolution and chaos. 1st ed. Saxo: Copenhagen, Denmark; 2013.
62. Van den Brink J, de Vries RP. Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol. 2011;91:1477-92.
63. Sánchez C. Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv. 2009;27:185-94.
64. Wang Y, Geer LY, Chappey C, Kans JA, Bryant SH. Cn3D: sequence and structure views for Entrez. Trends Biochem Sci. 2000;25:300-2.