Cellulose

, Volume 16, Issue 4, pp 723–727 | Cite as

Evidence for a novel mechanism of microbial cellulose degradation

Article

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.

Keywords

Cellulase Cellulosome Cytophaga hutchinsonii Fibrobacter succinogenes 

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 18:194–198Google Scholar
  4. Ding SY, Lamed R, Bayer EA, Himmel ME (2003) The bacterial scaffoldin: structure, function and potential applications in the nanosciences. Genet Eng (N Y) 25:209–225Google Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 98:399–413Google Scholar
  10. 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 1:1–8Google Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. Maglione G, Russell JB, Wilson DB (1997) Kinetics of Cellulose Digestion by Fibrobacter succinogenes S85. Appl Environ Microbiol 63:665–669Google Scholar
  15. 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 63:2449–2453Google Scholar
  16. 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 106:1954–1959Google Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 298:705–710Google Scholar
  20. Qi M, Jun HS, Forsberg CW (2007) Characterization and synergistic interactions of Fibrobacter succinogenes glycoside hydrolases. Appl Environ Microbiol 73:6098–6105CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. Spiridonov NA, Wilson DB (1998) Regulation of biosynthesis of individual cellulases in Thermomonospora fusca. J Bacteriol 180:3529–3532Google Scholar
  23. 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 26:173–178Google Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. Wilson DB (2004) Studies of Thermobifida fusca plant cell wall degrading enzymes. Chem Rec 4:72–82. doi:10.1002/tcr.20002 CrossRefGoogle Scholar
  27. Wilson DB (2008a) Aerobic microbial cellulase systems. Chap. 11. In: Himmel ME (ed) Biomass recalcitrance: deconstructing the plant cell wall for bioenergy. Blackwell, OxfordGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of Molecular Biology and GeneticsCornell UniversityIthacaUSA

Personalised recommendations