#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Analysis of the Genome, Transcriptome and Secretome Provides Insight into Its Pioneer Colonization Strategies of Wood


The wood decay fungus Phlebiopsis gigantea degrades all components of plant cell walls and is uniquely able to rapidly colonize freshly exposed conifer sapwood. However, mechanisms underlying its conversion of lignocellulose and resinous extractives have not been explored. We report here analyses of the genetic repertoire, transcriptome and secretome of P. gigantea. Numerous highly expressed hydrolases, together with lytic polysaccharide monooxygenases were implicated in P. gigantea's attack on cellulose, and an array of ligninolytic peroxidases and auxiliary enzymes were also identified. Comparisons of woody substrates with and without extractives revealed differentially expressed genes predicted to be involved in the transformation of resin. These expression patterns are likely key to the pioneer colonization of conifers by P. gigantea.


Vyšlo v časopise: Analysis of the Genome, Transcriptome and Secretome Provides Insight into Its Pioneer Colonization Strategies of Wood. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004759
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004759

Souhrn

The wood decay fungus Phlebiopsis gigantea degrades all components of plant cell walls and is uniquely able to rapidly colonize freshly exposed conifer sapwood. However, mechanisms underlying its conversion of lignocellulose and resinous extractives have not been explored. We report here analyses of the genetic repertoire, transcriptome and secretome of P. gigantea. Numerous highly expressed hydrolases, together with lytic polysaccharide monooxygenases were implicated in P. gigantea's attack on cellulose, and an array of ligninolytic peroxidases and auxiliary enzymes were also identified. Comparisons of woody substrates with and without extractives revealed differentially expressed genes predicted to be involved in the transformation of resin. These expression patterns are likely key to the pioneer colonization of conifers by P. gigantea.


Zdroje

1. BlanchetteR (1991) Delignification by wood-decay fungi. Ann Rev Phytopath 29: 381–398.

2. Eriksson K-EL, Blanchette RA, Ander P (1990) Microbial and enzymatic degradation of wood and wood components; Timell TE, editor. Berlin: Springer-Verlag.

3. Rayner ADM, Boddy L (1988) Fungal decomposition of wood: its biology and ecology. Chichester: John Wiley and Sons.

4. Kaarik AA (1974) Decomposition of wood. In: Dickinson CH, Pugh GJF, editors.Biology of plant litter composition.New York: Academic Press. pp.129–174.

5. ShigoAL (1967) Succession of organisms in discoloration and decay wood. Int Rev For Res 2: 237–299.

6. GutierrezA, Del RioJC, MartinezAT (2009) Microbial and enzymatic control of pitch in the pulp and paper industry. Appl Microbiol Biotechnol 82: 1005–1018.

7. Garbelotto M, Guglielmo F, Mascheretti S, Croucher PJ, Gonthier P (2013) Population genetic analyses provide insights on the introduction pathway and spread patterns of the North American forest pathogen Heterobasidion irregulare in Italy. Mol Ecol 10.1111/mec.12452.

8. RishbethJ (1963) Stump protection against Fomes annosus. Annals of Applied Biology 52: 63–77.

9. BehrendtCJ, BlanchetteRA (1997) Biological Processing of Pine Logs for Pulp and Paper Production with Phlebiopsis gigantea. Appl Environ Microbiol 63: 1995–2000.

10. BehrendtCJ, BlanchetteRA (2001) Biological control of blue stain in pulpwood: mechanisms of control used by Phlebiopsis gigantea. Holzforschung 55: 238–245.

11. FischerK, AkhtarM, BlanchetteRA, BurnesTA, MessnerK, et al. (1994) Reduction in resin content in wood chips during experimental biological pulping processes. Holzforschung 48: 285–290.

12. Martinez-InigoMJ, ImmerzeelP, GutierrezA, del RioJC, Sierra-AlvarezR (1999) Biodegradability of extractives in sapwood and heartwood from Scots Pine by sapstain and white rot fungi. Holzforschung 53: 247–252.

13. AdomasA, EklundM, JohanssonM, AsiegbuFO (2006) Identification and analysis of differentially expressed cDNAs during nonself-competitive interaction between Phlebiopsis gigantea and Heterobasidion parviporum. FEMS Microbiol Ecol 57: 26–39.

14. Kersten P, Cullen D (2013) Recent advances on the genomics of litter- and soil-inhabiting Agaricomycetes. Genomics of Soil- and Plant-Associated Fungi: Springer. pp. 311–332.

15. BaldrianP, ValaskovaV (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32: 501–521.

16. CantarelBL, CoutinhoPM, RancurelC, BernardT, LombardV, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233–238.

17. HoriC, GaskellJ, IgarashiK, SamejimaM, HibbettD, et al. (2013) Genome-wide analysis of polysaccharide degrading enzymes in eleven white- and brown-rot polyporales provides insight into mechanisms of wood decay. Mycologia 105: 1412–1427.

18. BeyM, ZhouS, PoidevinL, HenrissatB, CoutinhoPM, et al. (2013) Cello-oligosaccharide oxidation reveals differences between two lytic polysaccharide monooxygenases (family GH61) from Podospora anserina. Appl Environ Microbiol 79: 488–496.

19. QuinlanRJ, SweeneyMD, Lo LeggioL, OttenH, PoulsenJC, et al. (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci U S A 108: 15079–15084.

20. WesterengB, IshidaT, Vaaje-KolstadG, WuM, EijsinkVG, et al. (2011) The putative endoglucanase PcGH61D from Phanerochaete chrysosporium is a metal-dependent oxidative enzyme that cleaves cellulose. PLoS ONE 6: e27807.

21. FloudasD, BinderM, RileyR, BarryK, BlanchetteRA, et al. (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336: 1715–1719.

22. Fernandez-FueyoE, Ruiz-DuenasFJ, FerreiraP, FloudasD, HibbettDS, et al. (2012) Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc Natl Acad Sci U S A 109: 5458–5463.

23. MorgensternI, KlopmanS, HibbettDS (2008) Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes. J Mol Evol 66: 243–257.

24. KawaiS, AsukaiM, OhyaN, OkitaK, ItoT, et al. (1999) Degradation of non-phenolic beta-O-4 susbstructure and of polymeric lignin model compounds by laccase of Coriolus versicolor in the presence of 1-hydroxybenzotriazole. FEMS Microbiol Lett 170: 51–57.

25. BourbonnaisR, PaiceMG, FreiermuthB, BodieE, BornemanS (1997) Reactivities of various mediators and laccases with kraft pulp and lignin model compounds. Appl Environ Microbiol 63: 4627–4632.

26. EggertC, TempU, ErikssonK (1997) Laccase is essential for lignin degradation by the white-rot fungus Pycnoporus cinnabarinus. FEBS Lett 407: 89–92.

27. MartinezD, LarrondoLF, PutnamN, Sollewijn GelpkeMD, HuangK, et al. (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22: 695–700.

28. LarrondoL, SalasL, MeloF, VicunaR, CullenD (2003) A novel extracellular multicopper oxidase from Phanerochaete chrysosporium with ferroxidase activity. Appl Environ Microbiol 69: 6257–6263.

29. HoeggerPJ, KilaruS, JamesTY, ThackerJR, KüesU (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273: 2308–2326.

30. LevasseurA, DrulaE, LombardV, CoutinhoPM, HenrissatB (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6: 41.

31. BastianS, RekowskiMJ, WitteK, Heckmann-PohlDM, GiffhornF (2005) Engineering of pyranose 2-oxidase from Peniophora gigantea towards improved thermostability and catalytic efficiency. Appl Microbiol Biotechnol 67: 654–663.

32. YadavJS, SoellnerMB, LoperJC, MishraPK (2003) Tandem cytochrome P450 monooxygenase genes and splice variants in the white rot fungus Phanerochaete chrysosporium: cloning, sequence analysis, and regulation of differential expression. Fungal Genet Biol 38: 10–21.

33. SyedK, PorolloA, LamYW, GrimmettPE, YadavJS (2013) CYP63A2, a catalytically versatile fungal P450 monooxygenase capable of oxidizing higher-molecular-weight polycyclic aromatic hydrocarbons, alkylphenols, and alkanes. Appl Environ Microbiol 79: 2692–2702.

34. SyedK, YadavJS (2012) P450 monooxygenases (P450ome) of the model white rot fungus Phanerochaete chrysosporium. Crit Rev Microbiol 38: 339–363.

35. DowdCA, BuckleyCM, SheehanD (1997) Glutathione S-transferases from the white-rot fungus, Phanerochaete chrysosporium. Biochem J 324 (Pt 1): 243–248.

36. ReiserJ, MuheimA, HardeggerM, FrankG, FiechterA (1994) Aryl-alcohol dehydrogenase from the white-rot fungus Phanerochaete chrysosporium: gene cloning, sequence analysis, expression and purification of recombinant protein. J Biol Chem 269: 28152–28159.

37. HibbettDS, DonoghueMJ (2001) Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50: 215–242.

38. GrigorievIV, NordbergH, ShabalovI, AertsA, CantorM, et al. (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40: D26–32.

39. RileyR, SalamovAA, BrownDW, NagyLG, FloudasD, et al. (2014) Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci U S A 111: 9923–9928.

40. Sjöström E (1993) Wood Chemistry. Fundamentals and Applications. San Diego: Academic Press. 293 p.

41. KerstenPJ (1990) Glyoxal oxidase of Phanerochaete chrysosporium: Its characterization and activation by lignin peroxidase. Proc Natl Acad Sci USA 87: 2936–2940.

42. de KokerTH, MozuchMD, CullenD, GaskellJ, KerstenPJ (2004) Pyranose 2-oxidase from Phanerochaete chrysosporium: isolation from solid substrate, protein purification, and characterization of gene structure and regulation. Appl Environ Microbiol 70: 5794–5800.

43. GiffhornF (2000) Fungal pyranose oxidases: occurrence, properties and biotechnical applications in carbohydrate chemistry. Appl Microbiol Biotechnol 54: 727–740.

44. SunHW, PlappBV (1992) Progressive sequence alignment and molecular evolution of the Zn-containing alcohol dehydrogenase family. J Mol Evol 34: 522–535.

45. MartinezD, ChallacombeJ, MorgensternI, HibbettD, SchmollM, et al. (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 106: 1954–1959.

46. EastwoodDC, FloudasD, BinderM, MajcherczykA, SchneiderP, et al. (2011) The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333: 762–765.

47. LangstonJA, ShaghasiT, AbbateE, XuF, VlasenkoE, et al. (2011) Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol 77: 7007–7015.

48. PhillipsCM, BeesonWT, CateJH, MarlettaMA (2011) Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol 6: 1399–1406.

49. MacdonaldJ, DoeringM, CanamT, GongY, GuttmanDS, et al. (2011) Transcriptomic responses of the softwood-degrading white-rot fungus Phanerochaete carnosa during growth on coniferous and deciduous wood. Appl Environ Microbiol 77: 3211–3218.

50. DoradoJ, ClaassenFW, van BeekTA, LenonG, WijnbergJB, et al. (2000) Elimination and detoxification of softwood extractives by white-rot fungi. J Biotechnol 80: 231–240.

51. GutierrezA, del RioJC, Gonzalez-VilaFJ, MartinF (1998) Analysis of lipophilic extractives from wood and pitch deposits by solid-phase extraction and gas chromatography. J Chromatogr 823: 449–455.

52. IshihamaY, OdaY, TabataT, SatoT, NagasuT, et al. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265–1272.

53. DanielG, VolcJ, FilonovaL, PlihalO, KubatovaE, et al. (2007) Characteristics of Gloeophyllum trabeum alcohol oxidase, an extracellular source of H2O2 in brown rot decay of wood. Appl Environ Microbiol 73: 6241–6253.

54. BendtsenJD, JensenLJ, BlomN, Von HeijneG, BrunakS (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein engineering, design & selection: PEDS 17: 349–356.

55. van BeekTA, ClaassenFW, DoradoJ, GodejohannM, Sierra-AlvarezR, et al. (2007) Fungal biotransformation products of dehydroabietic acid. J Nat Prod 70: 154–159.

56. AdamsAS, AylwardFO, AdamsSM, ErbilginN, AukemaBH, et al. (2013) Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol 79: 3468–3475.

57. KumarSV, PhalePS, DuraniS, WangikarPP (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83: 386–394.

58. HofrichterM, UllrichR, PecynaMJ, LiersC, LundellT (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol 87: 871–897.

59. LiersC, PecynaMJ, KellnerH, WorrichA, ZornH, et al. (2013) Substrate oxidation by dye-decolorizing peroxidases (DyPs) from wood- and litter-degrading agaricomycetes compared to other fungal and plant heme-peroxidases. Appl Microbiol Biotechnol 97: 5839–5849.

60. Agger JW, Isaksen T, Varnai A, Vidal-Melgosa S, Willats WG, et al. (2014) Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci U S A 10.1073/pnas.1323629111.

61. Vaaje-KolstadG, WesterengB, HornSJ, LiuZ, ZhaiH, et al. (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330: 219–222.

62. Vanden WymelenbergA, MingesP, SabatG, MartinezD, AertsA, et al. (2006) Computational analysis of the Phanerochaete chrysosporium v2.0 genome database and mass spectrometry identification of peptides in ligninolytic cultures reveals complex mixtures of secreted proteins. Fungal Genet Biol 43: 343–356.

63. WangY, LimL, DiGuistiniS, RobertsonG, BohlmannJ, et al. (2013) A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytol 197: 886–898.

64. MatsuzakiF, ShimizuM, WariishiH (2008) Proteomic and metabolomic analyses of the white-rot fungus Phanerochaete chrysosporium exposed to exogenous benzoic acid. J Proteome Res 7: 2342–2350.

65. ShimizuM, YudaN, NakamuraT, TanakaH, WariishiH (2005) Metabolic regulation at the tricarboxylic acid and glyoxylate cycles of the lignin-degrading basidiomycete Phanerochaete chrysosporium against exogenous addition of vanillin. Proteomics 5: 3919–3931.

66. AnnesiT, CurcioG, D'AmicoL, MottaE (2005) Biological control of Heterobasidion annosum on Pinus pinea by Phlebiopsis gigantea. Forest Pathology 35: 127–134.

67. MunirE, YoonJJ, TokimatsuT, HattoriT, ShimadaM (2001) A physiological role for oxalic acid biosynthesis in the wood-rotting basidiomycete Fomitopsis palustris. Proc Natl Acad Sci USA 98: 11126–11130.

68. BlanchetteRA, HeldBW, ArenzBE, JurgensJA, BaltesNJ, et al. (2010) An Antarctic hot spot for fungi at Shackleton's historic hut on Cape Royds. Microb Ecol 60: 29–38.

69. Grigoriev IV, Martinez DA, Salamov AA (2006) Fungal genomic annotation. In: Arora DK, Berka RA, Singh GB, editors.Applied Mycology and Biotechnology.Amsterdam: Elsevier. pp. 123–142.

70. ParraG, BradnamK, KorfI (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23: 1061–1067.

71. Vanden WymelenbergA, GaskellJ, MozuchMD, SabatG, RalphJ, et al. (2010) Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium. Appl Environ Microbiol 76: 3599–3610.

72. RyuJS, SharyS, HoutmanCJ, PaniskoEA, KorripallyP, et al. (2011) Proteomic and functional analysis of the cellulase system expressed by Postia placenta during brown rot of solid wood. Appl Environ Microbiol 77: 7933–7941.

73. NesvizhskiiAI, KellerA, KolkerE, AebersoldR (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646–4658.

74. Vanden WymelenbergA, GaskellJ, MozuchMD, KerstenP, SabatG, et al. (2009) Transcriptome and secretome analysis of Phanerochaete chrysosporium reveal complex patterns of gene expression. Appl Environ Microbiol 75: 4058–4068.

75. OlsonA, AertsA, AsiegbuF, BelbahriL, BouzidO, et al. (2012) Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. New Phytol 194: 1001–1013.

76. Vanden WymelenbergA, SabatG, MozuchMD, KerstenP, CullenD, et al. (2006) Structure, organization, and transcriptional regulation of a family of copper radical oxidase genes in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 72: 4871–4877.

77. AspeborgH, CoutinhoPM, WangY, BrumerH3rd, HenrissatB (2012) Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 12: 186.

78. RzhetskyA, NeiM (1992) Statistical properties of the ordinary least-squares, generalized least-squares, and minimum-evolution methods of phylogenetic inference. J Mol Evol 35: 367–375.

79. Zuckerkandl J, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ, editors.Evolving genes and proteins. New York: Academic Press.

80. SaitouN, NeiM (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.

81. TamuraK, DudleyJ, NeiM, KumarS (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.

82. GuillenF, EvansCS (1994) Anisaldehyde and veratraldehyde acting as redox cycling agents for H2O2 production by Pleurotus eryngii. Appl Environ Microbiol 60: 2811–2817.

83. FerreiraP, Ruiz-DuenasFJ, MartinezMJ, van BerkelWJ, MartinezAT (2006) Site-directed mutagenesis of selected residues at the active site of aryl-alcohol oxidase, an H2O2-producing ligninolytic enzyme. FEBS J 273: 4878–4888.

84. CavenerDR (1992) GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J Mol Biol 223: 811–814.

85. ThompsonJD, HigginsDG, GibsonTJ (1994) ClustalW improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 2552–2556.

86. HallbergBM, HenrikssonG, PetterssonG, VasellaA, DivneC (2003) Mechanism of the reductive half-reaction in cellobiose dehydrogenase. J Biol Chem 278: 7160–7166.

87. LetteraV, PiscitelliA, LeoG, BiroloL, PezzellaC, et al. (2010) Identification of a new member of Pleurotus ostreatus laccase family from mature fruiting body. Fungal Biol 114: 724–730.

88. KilaruS, HoeggerPJ, KüesU (2006) The laccase multi-gene family in Coprinopsis cinerea has seventeen different members that divide into two distinct subfamilies. Curr Genet 50: 45–60.

89. RühlM, MajcherczykA, KuesU (2013) Lcc1 and Lcc5 are the main laccases secreted in liquid cultures of Coprinopsis cinerea strains. Antonie van Leeuwenhoek 103: 1029–1039.

90. KüesU, RühlM (2011) Multiple multi-copper oxidase gene families in basidiomycetes - what for? Curr Genomics 12: 72–94.

91. AltschulSF, MaddenTL, SchafferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

92. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#