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Evidence for a novel mechanism of microbial cellulose degradation

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Abstract

There are two well studied mechanisms that are used by cellulolytic microorganisms to degrade the cellulose present in plant cell walls and a third less well studied oxidative mechanism used by brown rot fungi. The well studied mechanisms use cellulases to hydrolyze the β-1,4 linkages present in cellulose, however the way in which cellulases are presented to the environment are quite different for each mechanism. Most aerobic microorganisms secrete a set of cellulases outside the cell (free cellulase mechanism) while most anaerobic microorganisms produce large multi enzyme complexes on their outer surface (cellulosomal mechanism). Their genomic sequences suggest that the aerobic bacterium, Cytophaga hutchinsonii and the anaerobic bacterium, Fibrobacter succinogenes, do not use either of these mechanisms for degrading cellulose, as these organisms only code for normal endocellulases not for processive cellulases like exocellulases and processive endocellulases which are used in both of the well studied mechanisms.

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References

  • Bayer EA, Belaich JP, Shoham Y, Lamed R (2004) The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol 58:521–554. doi:10.1146/annurev.micro.57.030502.091022

    Article  CAS  Google Scholar 

  • Carvalho AL, Goyal A, Prates JA, Bolam DN, Gilbert HJ, Pires VM, Ferreira LM, Planas A, Romao MJ, Fontes CM (2004) The family 11 carbohydrate-binding module of Clostridium thermocellum Lic26A-Cel5E accommodates beta-1, 4- and beta-1, 3-1, 4-mixed linked glucans at a single binding site. J Biol Chem 279:34785–34793. doi:10.1074/jbc.M405867200

    Article  CAS  Google Scholar 

  • Chen X, Zeng Y, Jiao N (2008) Characterization of Cytophaga-Flavobacteria community structure in the Bering Sea by cluster-specific 16S rRNA gene amplification analysis. J Microbiol Biotechnol 18:194–198

    CAS  Google Scholar 

  • Ding SY, Lamed R, Bayer EA, Himmel ME (2003) The bacterial scaffoldin: structure, function and potential applications in the nanosciences. Genet Eng (N Y) 25:209–225

    Google Scholar 

  • Fields MW, Mallik S, Russell JB (2000) Fibrobacter succinogenes S85 ferments ball-milled cellulose as fast as cellobiose until cellulose surface area is limiting. Appl Microbiol Biotechnol 54:570–574. doi:10.1007/s002530000426

    Article  CAS  Google Scholar 

  • Fierobe HP, Mingardon F, Mechaly A, Bélaïch A, Rincon MT, Pagès S, Lamed R, Tardif C, Bélaïch JP, Bayer EA (2005) Action of designer cellulosomes on homogeneous versus complex substrates: controlled incorporation of three distinct enzymes into a defined trifunctional scaffoldin. J Biol Chem 280:16325–16334. doi:10.1074/jbc.M414449200

    Article  CAS  Google Scholar 

  • Gilad R, Rabinovich L, Yaron S, Bayer EA, Lamed R, Gilbert HJ, Shoham Y (2003) CelI, a noncellulosomal family 9 enzyme from Clostridium thermocellum, is a processive endoglucanase that degrades crystalline cellulose. J Bacteriol 18:391–398. doi:10.1128/JB.185.2.391-398.2003

    Article  CAS  Google Scholar 

  • Han SO, Yukawa H, Inui M, Doi RH (2005) Molecular cloning and transcriptional and expression analysis of engO, encoding a new noncellulosomal family 9 enzyme, from Clostridium cellulovorans. J Bacteriol 187:4884–4889. doi:10.1128/JB.187.14.4884-4889.2005

    Article  CAS  Google Scholar 

  • Hashimoto W, Yamasaki M, Itoh T, Momma K, Mikami B, Murata K (2004) Super-channel in bacteria: structural and functional aspects of a novel biosystem for the import and depolymerization of macromolecules. J Biosci Bioeng 98:399–413

    CAS  Google Scholar 

  • Hastie PM, Mitchell K, Murray JA (2008) Semi-quantitative analysis of Ruminococcus flavefaciens, Fibrobacter succinogenes and Streptococcus bovis in the equine large intestine using real-time polymerase chain reaction. Br J Nutr 1:1–8

    Google Scholar 

  • Irwin DC, Spezio M, Walker LP, Wilson DB (1993) Activity studies of eight purified cellulases: specificity, synergism, and binding domain effects. Biotechnol Bioeng 42:1002–1013. doi:10.1002/bit.260420811

    Article  CAS  Google Scholar 

  • Jun HS, Qi M, Gong J, Egbosimba EE, Forsberg CW (2007) Outer membrane proteins of Fibrobacter succinogenes with potential roles in adhesion to cellulose and in cellulose digestion. J Bacteriol 189:6806–6815. doi:10.1128/JB.00560-07

    Article  CAS  Google Scholar 

  • Kobayashi Y, Shinkai T, Koike S (2008) Ecological and physiological characterization shows that Fibrobacter succinogenes is important in rumen fiber digestion. Folia Microbiol (Praha) 53:195–200. doi:10.1007/s12223-008-0024-z

    Article  CAS  Google Scholar 

  • Maglione G, Russell JB, Wilson DB (1997) Kinetics of Cellulose Digestion by Fibrobacter succinogenes S85. Appl Environ Microbiol 63:665–669

    CAS  Google Scholar 

  • Malburg SR, Malburg LM Jr, Liu T, Iyo AH, Forsberg CW (1997) Catalytic properties of the cellulose-binding endoglucanase F from Fibrobacter succinogenes S85. Appl Environ Microbiol 63:2449–2453

    CAS  Google Scholar 

  • Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Vanden Wymelenberg A, Gaskell J, Lindquist E, Sabat G, Bondurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavín JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kües U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954–1959

  • McDonald JE, Lockhart RJ, Cox MJ, Allison HE, McCarthy AJ (2008) Detection of novel fibrobacter populations in landfill sites and determination of their relative abundance via quantitative PCR. Environ Microbiol 10:1310–1319. doi:10.1111/j.1462-2920.2007.01544.x

    Article  CAS  Google Scholar 

  • Munshi TK, Chattoo BB (2008) Bacterial population structure of the jute-retting environment. Microb Ecol 56:270–282. doi:10.1007/s00248-007-9345-8

    Article  Google Scholar 

  • Nidetzky B, Steiner W, Hayn M, Claeyssens M (1994) Cellulose hydrolysis by the cellulases from Trichoderma reesei: a new model for synergistic interaction. Biochem J 298:705–710

    CAS  Google Scholar 

  • Qi M, Jun HS, Forsberg CW (2007) Characterization and synergistic interactions of Fibrobacter succinogenes glycoside hydrolases. Appl Environ Microbiol 73:6098–6105

    Article  CAS  Google Scholar 

  • Shipman JA, Berleman JE, Salyers AA (2000) Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J Bacteriol 182:5365–5372. doi:10.1128/JB.182.19.5365-5372.2000

    Article  CAS  Google Scholar 

  • Spiridonov NA, Wilson DB (1998) Regulation of biosynthesis of individual cellulases in Thermomonospora fusca. J Bacteriol 180:3529–3532

    CAS  Google Scholar 

  • Teeri TT, Koivula A, Linder M, Wohlfahrt G, Divne C, Jones TA (1998) Trichoderma reesei cellobiohydrolases: why so efficient on crystalline cellulose? Biochem Soc Trans 26:173–178

    CAS  Google Scholar 

  • Tomme P, Warren RA, Gilkes NR (1995) Cellulose hydrolysis by bacteria and fungi. Adv Microb Physiol 37:1–81. doi:10.1016/S0065-2911(08)60143-5

    Article  CAS  Google Scholar 

  • Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernández M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565. doi:10.1038/nature06269

    Article  CAS  Google Scholar 

  • Wilson DB (2004) Studies of Thermobifida fusca plant cell wall degrading enzymes. Chem Rec 4:72–82. doi:10.1002/tcr.20002

    Article  CAS  Google Scholar 

  • Wilson DB (2008a) Aerobic microbial cellulase systems. Chap. 11. In: Himmel ME (ed) Biomass recalcitrance: deconstructing the plant cell wall for bioenergy. Blackwell, Oxford

    Google Scholar 

  • Wilson DB (2008b) Three microbial strategies for plant cell wall degradation. Ann N Y Acad Sci 1125:289–297. doi:10.1196/annals.1419.026

    Article  CAS  Google Scholar 

  • Xie G, Bruce DC, Challacombe JF, Chertkov O, Detter JC, Gilna P, Han CS, Lucas S, Misra M, Myers GL, Richardson P, Tapia R, Thayer N, Thompson LS, Brettin TS, Henrissat B, Wilson DB, McBridge MJ (2007) Genome sequence of the cellulolytic gliding bacterium Cytophaga hutchinsonii. Appl Environ Microbiol 73:3536–3546. doi:10.1128/AEM.00225-07

    Article  CAS  Google Scholar 

  • Zverlov VV, Schwarz WH (2008) Bacterial cellulose hydrolysis in anaerobic environmental subsystems—Clostridium thermocellum and Clostridium stercorarium, thermophilic plant-fiber degraders. Ann N Y Acad Sci 1125:298–307. doi:10.1196/annals.1419.008

    Article  CAS  Google Scholar 

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  1. Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, 14853, USA

    David B. Wilson

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Correspondence to David B. Wilson.

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Wilson, D.B. Evidence for a novel mechanism of microbial cellulose degradation. Cellulose 16, 723–727 (2009). https://doi.org/10.1007/s10570-009-9326-9

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  • DOI: https://doi.org/10.1007/s10570-009-9326-9

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