DOI QR코드

DOI QR Code

Fibrobacter succinogenes, a Dominant Fibrolytic Ruminal Bacterium: Transition to the Post Genomic Era

  • Jun, H.S. (Department of Molecular and Cellular Biology, University of Guelph) ;
  • Qi, M. (Department of Molecular and Cellular Biology, University of Guelph) ;
  • Ha, J.K. (School of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University) ;
  • Forsberg, C.W. (Department of Molecular and Cellular Biology, University of Guelph)
  • 발행 : 2007.05.01

초록

Fibrobacter succinogenes, a Gram-negative, anaerobic ruminal bacterium is a major fibre digesting species in the rumen. It intensively degrades plant cell walls by an erosion type of mechanism, burrowing its way through the complex matrix of cellulose and hemicellulose with the release of digestible and undigested cell wall fragments. The enzymes involved in this process include a combination of glucanases, xylanases, arabinofuranosidase(s) and esterases. The genome of the bacterium has been sequenced and this has revealed in excess of 100 putative glycosyl hydrolase, pectate lyase and carbohydrate esterase genes, which is greater than the numbers reported present in other major cellulolytic organisms for which genomes have been sequenced. Modelling of the amino acid sequences of two glycanases, CedA and EGB, by reference to crystallized homologs has enabled prediction of the major features of their tertiary structures. Two dimensional gel electrophoresis in conjunction with mass spectroscopy has permitted the documentation of proteins over expressed in F. succinogenes grown on cellulose, and analysis of the cell surfaces of mutant strains unable to bind to cellulose has enabled the identification of candidate proteins with roles in adhesion to the plant cell wall substrate, the precursor to cellulose biodegradation.

키워드

참고문헌

  1. Amann, R. I., C. Lin, R. Key, L. Montgomery and D. A. Stahl. 1992. Diversity among Fibrobacter isolates: Towards a phylogenetic classification. Syst. Appl. Microbiol. 15:23-31. https://doi.org/10.1111/j.1472-765X.1992.tb00714.x
  2. Barriere, Y., C. Guillet, D. Goffner and M. Pichon. 2003. Genetic variation and breeding strategies for improved cell wall digestibility in annual forage crops. Anim. Res. 52:193-228. https://doi.org/10.1051/animres:2003018
  3. Bera-Maillet, C., Y. Ribot and E. Forano. 2004. Fiber-degrading systems of different strains of the genus Fibrobacter. Appl. Environ. Microbiol. 70:2172-2179. https://doi.org/10.1128/AEM.70.4.2172-2179.2004
  4. Bourquin, L. D. and G. C. Fahey, Jr. 1994. Ruminal digestion and glycosyl linkage patterns of cell wall components from leaf and stem fractions of alfalfa, orchardgrass, and wheat straw. J. Anim. Sci. 72:1362-1374. https://doi.org/10.2527/1994.7251362x
  5. Broussolle, V., E. Forano, G. Gaudet and Y. Ribot. 1994. Gene sequence and analysis of protein domains of EGB, a novel family E endoglucanase from S85. FEMS Microbiol. Lett. 124:439-447. https://doi.org/10.1111/j.1574-6968.1994.tb07321.x
  6. Casler, M. D., D. R. Buxton and K. P. Vogel. 2002. Genetic modification of lignin concentration affects fitness of perennial herbaceous plants. Theor. Appl. Genet. 104:127-131. https://doi.org/10.1007/s001220200015
  7. Cheng, K.-J., C. S. Stewart, D. Dinsdale and J. W. Costerton. 1983. Electron microscopy of bacteria involved in the digesion of plant cell walls. Anim. Feed Sci. Technol. 10:93-120. https://doi.org/10.1016/0377-8401(84)90002-6
  8. Cosgrove, D. J. 2005. Growth of the plant cell wall. Nat. Rev. Mol. Cell. Biol. 6:850-861. https://doi.org/10.1038/nrm1746
  9. Dehority, B. A. and P. A. Tirabasso. 1998. Effect of ruminal cellulolytic bacterial concentrations on in situ digestion of forage cellulose. J. Anim. Sci. 76:2905-2911. https://doi.org/10.2527/1998.76112905x
  10. Doi, R. H. and A. Kosugi. 2004. Cellulosomes: plant-cell-walldegrading enzyme complexes. Nat. Rev. Microbiol. 2:541-551. https://doi.org/10.1038/nrmicro925
  11. Dominguez, R., H. Souchon, M. B. Lascombe and P. M. Alzari. 1996. The crystal structure of a family 5 endoglucanase mutant in complexed and uncomplexed forms reveals an induced fit activation mechanism. J. Mol. Biol. 257:1042-1051. https://doi.org/10.1006/jmbi.1996.0222
  12. Forano, E., V. Broussolle, G. Gaudet and J. A. Bryant. 1994. Molecular cloning, expression, and characterization of a new endoglucanase gene from Fibrobacter succinogenes S85. Curr. Microbiol. 28:7-14. https://doi.org/10.1007/BF01575979
  13. Forsberg, C. W., K.-J. Cheng and B. A. White. 1997. Polysaccharide degradation in the rumen and large intestine. In: Gastrointestinal Microbiology (Ed. R. I. Mackie and B. A. White). Chapman and Hall. New York. pp. 319-379.
  14. Forsberg, C. W., E. Forano and A. Chesson. 2000. Microbial adherence to plant cell wall and enzymatic hydrolysis. In: Ruminant physiology digestion, metabolism, growth and reproduction (Ed. P. B. Cronje). CABI Publishing. Wallingford, Oxon. pp. 79-98.
  15. Gardner, P. T., T. M. Wood, A. Chesson and T. Stuchbury. 1999. Effect of degradation on the porosity and surface area of forage cell walls of differing lignin content. J. Sci. Food Agric. 79:11-18. https://doi.org/10.1002/(SICI)1097-0010(199901)79:1<11::AID-JSFA159>3.0.CO;2-6
  16. Gong, J. and C. W. Forsberg. 1989. Factors affecting adhesion of Fibrobacter succinogenes subsp. succinogenes S85 and adherence-defective mutants to cellulose. Appl. Environ. Microbiol. 55:3039-3044.
  17. Grabber, J. H., J. Ralph, C. Lapierre and Y. Barriere. 2004. Genetic and molecular basis of grass cell-wall degradability. I. Lignincell wall matrix interactions. C. R. Biol. 327:455-465. https://doi.org/10.1016/j.crvi.2004.02.009
  18. Huang, L. and C. W. Forsberg. 1987. Isolation of a cellodextrinase from Bacteroides succinogenes. Appl. Environ. Microbiol. 54:1488-1493.
  19. Huhtanen, P., S. Ahvenjarvi, M. R. Weisbjerg and P. NOrgaard. 2006. Digestion and passage of fibre in ruminants. In: Ruminant physiology: Digestion, metabolism and impact of nutrition on gene expression, immunology and stress (Ed. K. Sejrsen, T. Hvelplund and M. O. Nielsen). Wageningen Academic Publishers. Wageningen. pp. 87-135
  20. Iyo, A. H. and C. W. Forsberg. 1994. Features of the cellodextrinase gene from Fibrobacter succinogenes S85. Can. J. Microbiol. 40:592-596. https://doi.org/10.1139/m94-094
  21. Jun, H. S., J. K. Ha, L. M. Malburg, Jr., A. M. Verrinder Gibbins and C. W. Forsberg. 2003. Characteristics of a cluster of xylanase genes in Fibrobacter succinogenes S85. Can. J. Microbiol. 49:171-180. https://doi.org/10.1139/w03-024
  22. Kam, D. K., H. S. Jun, J. Ha, G. D. Inglis and C. W. Forsberg. 2005. Characteristics of adjacent family 6 acetylxylan esterases from Fibrobacter succinogenes and the interaction with the XynE xylanase in hydrolysis of acetylated xylan. Can. J. Microbiol. 51:821-832. https://doi.org/10.1139/w05-074
  23. Koike, S., J. Pan, T. Suzuki, T. Takano, C. Oshima, Y. Kobayashi and K. Tanaka. 2004. Ruminal distribution of the cellulolytic bacterium Fibrobacter succinogenes in relation to its phylogenetic grouping. Anim. Sci. J. 75:417-422. https://doi.org/10.1111/j.1740-0929.2004.00207.x
  24. Koike, S., J. Pan, Y. Kobayashi and K. Tanaka. 2003. Kinetics of in sacco fiber-attachment of representative ruminal cellulolytic bacteria monitored by competitive PCR. J. Dairy Sci. 86:1429-1435. https://doi.org/10.3168/jds.S0022-0302(03)73726-6
  25. Krause, D. O., S. E. Denman, R. I. Mackie, M. Morrison, A. L. Rae, G. T. Attwood and C. S. McSweeney. 2003. Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiol. Rev. 27:663-693. https://doi.org/10.1016/S0168-6445(03)00072-X
  26. Lynd, L. R., P. J. Weimer, W. H. van Zyl and I. S. Pretorius. 2002. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 66: 506-577. https://doi.org/10.1128/MMBR.66.3.506-577.2002
  27. Maglione, G., J. B. Russell and D. B. Wilson. 1997. Kinetics of cellulose digestion by Fibrobacter succinogenes S85. Appl. Environ. Microbiol. 63:665-669.
  28. Malburg, S. R. C., L. M. Malburg, T. Liu, A. H. Iyo and C. W. Forsberg. 1997. Catalytic properties of the cellulose-binding endoglucanase F from Fibrobacter succinogenes S85. Appl. Environ. Microbiol. 63:2449-2453.
  29. Matte, A., C. W. Forsberg and A. M. Verrinder Gibbins. 1992a. Enzymes associated with metabolism of xylose and other pentoses by Prevotella (Bacteroides) ruminicola strains, Selenomonas ruminantium D, and Fibrobacter succinogenes S85. Can. J. Microbiol. 38:370-376, 1992. https://doi.org/10.1139/m92-063
  30. Matte, A. and C. W. Forsberg. 1992b. Purification, characterization, and mode of action of endoxylanases 1 and 2 from Fibrobacter succinogenes S85. Appl. Environ. Microbiol. 58:157-168.
  31. Matulova, M., R. Nouaille, P. Capek, M. Pean, E. Forano and A. M. Delort. 2005. Degradation of wheat straw by Fibrobacter succinogenes S85: a liquid- and solid-state nuclear magnetic resonance study. Appl. Environ. Microbiol. 71:1247-1253. https://doi.org/10.1128/AEM.71.3.1247-1253.2005
  32. McDermid, K. P., C. W. Forsberg and C. R. MacKenzie. 1990a. Purification and properties of an acetylxylan esterase from Fibrobacter succinogenes S85. Appl. Environ. Microbiol. 56:3805-3810.
  33. McDermid, K. P., C. R. MacKenzie and C. W. Forsberg. 1990b. Esterase activities of Fibrobacter succinogenes subsp. succinogenes S85. Appl. Environ. Microbiol. 56:127-132.
  34. Michalet-Doreau, B., I. Fernandez, C. Peyron, L. Millet and G. Fonty. 2001. Fibrolytic activities and cellulolytic bacterial community structure in the solid and liquid phases of rumen contents. Reprod. Nutr. Dev. 41:187-194. https://doi.org/10.1051/rnd:2001122
  35. Miron, J. and C. W. Forsberg. 1998. Features of Fibrobacter intestinalis DR7 mutant which is impaired with its ability to adhere to cellulose. Anaerobe 74:35-43.
  36. Miron, J. and C. W. Forsberg. 1999. Characterisation of cellulosebinding proteins which are involved in adhesion mechanism of Fibrobacter intestinalis DR7. Appl. Microbiol. Biotechnol. 51:491-497. https://doi.org/10.1007/s002530051422
  37. Morrison, M., K. E. Nelson, I. Cann, C. W. Forsberg, R. I. Mackie, J. B. Russell, B. A. White, D. B. Wilson, K. Amya, B. Cheng, S. Qi, H.-S. Jun, S. Mulligan, K. Tran, H. Carty, H. Khouri, W. Nelson, S. Daugherty and C. Fraser. 2003. The Fibrobacter succinogenes strain S85 sequencing project. 3rd ASM-TIGR, Microbial Genome Meeting,New Orleans.
  38. Ozutsumi, Y., K. Tajima, A. Takenaka and H. Itabashi. 2006. Realtime PCR detection of the effects of protozoa on rumen bacteria in cattle. Curr. Microbiol. 52:158-162. https://doi.org/10.1007/s00284-005-0266-9
  39. Qi, M., K. E. Nelson, S. C. Daugherty, W. C. Nelson, I. R. Hance, M. Morrison and C. W. Forsberg. 2005. Novel molecular features of the fibrolytic intestinal bacterium Fibrobacter intestinalis not shared with Fibrobacter succinogenes as determined by suppressive subtractive hybridization. J. Bacteriol. 187:3739-3751. https://doi.org/10.1128/JB.187.11.3739-3751.2005
  40. Reznikoff, W. S., I. Y. Goryshin and J. J. Jendrisak. 2004. Tn5 as a molecular genetics tool: In vitro transposition and the coupling of in vitro technologies with in vivo transposition. In: Mobile genetic elements: Protocols and genomic applications. (Anonymous). Humana Press. Totowa, NJ. pp. 83-96.
  41. Satter, L. D., H. G. Jung, A. M. van Vuuren and F. M. Engels. 1999. Challenges in the nutrition of high-producing ruminants. In: Nutritional ecology of herbivores. (Ed. H. J. G. Jung and G. C. Fahey, Jr.). Proceedings of the Vth international symposium on the nutrition of herbivores. pp. 609-649.
  42. Schwede, T., J. Kopp, N. Guex and M. C. Peitsch. 2003. SWISS MODEL: an automated protein homology-modeling server. Nucl. Acids Res. 31:3381-3385. https://doi.org/10.1093/nar/gkg520
  43. Schubot, F. D., I. A. Kataeva, J. Chang, A. K. Shah, L. G. Ljungdahl, J. P. Rose, and B. C. Wang. 2004. Structural basis for the exocellulase activity of the cellobiohydrolase CbhA from Clostridium thermocellum. Biochemistry 43:1163-1170. https://doi.org/10.1021/bi030202i
  44. Smith, D. C. and C. W. Forsberg. 1991. $\alpha$-Glucuronidase and other hemicellulase activities of Fibrobacter succinogenes S85 grown on crystalline cellulose or ball-milled barley straw. Appl. Environ. Microbiol. 57:3552-3557.
  45. Tsai, L. C., L. F. Shyur, Y. S. Cheng and S. L. Lee. 2005. Crystal structure of truncated Fibrobacter succinogenes 1,3-1,4-$\beta$-Dglucanase in complex with $\alpha$-1,3-1,4-cellotriose. J. Mol. Biol. 354:642-651. https://doi.org/10.1016/j.jmb.2005.09.041
  46. Wells, J. E., J. B. Russell, Y. Shi and P. J. Weimer. 1995. Cellodextrin efflux by the cellulolytic ruminal bacterium Fibrobacter succinogenes and its potential role in the growth of nonadherent bacteria. Appl. Environ. Microbiol. 61:1757-1762.
  47. Wood, T. M. and S. I. McCrae. 1986. The effect of acetyl groups on the hydrolysis of ryegrass cell walls by xylanase and cellulase from Trichoderma koningii. Phytochemistry 25:1053-1055. https://doi.org/10.1016/S0031-9422(00)81552-6

피인용 문헌

  1. Application of rumen microbial genome information to livestock systems in the postgenomic era vol.48, pp.7, 2008, https://doi.org/10.1071/EA07408
  2. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis vol.6, pp.2, 2008, https://doi.org/10.1038/nrmicro1817
  3. The Glycobiome of the Rumen Bacterium Butyrivibrio proteoclasticus B316T Highlights Adaptation to a Polysaccharide-Rich Environment vol.5, pp.8, 2010, https://doi.org/10.1371/journal.pone.0011942
  4. The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist vol.6, pp.4, 2011, https://doi.org/10.1371/journal.pone.0018814
  5. The Early Impact of Genomics and Metagenomics on Ruminal Microbiology vol.3, pp.1, 2015, https://doi.org/10.1146/annurev-animal-022114-110705
  6. Metagenomic analysis reveals the influences of milk containing antibiotics on the rumen microbes of calves vol.199, pp.3, 2017, https://doi.org/10.1007/s00203-016-1311-8
  7. A global analysis of gene expression in Fibrobacter succinogenes S85 grown on cellulose and soluble sugars at different growth rates vol.11, pp.1, 2018, https://doi.org/10.1186/s13068-018-1290-x
  8. In vitro evaluation of Rhus succedanea extracts for ruminants vol.31, pp.10, 2018, https://doi.org/10.5713/ajas.18.0045
  9. Ecological and physiological characterization shows that Fibrobacter succinogenes is important in rumen fiber digestion - Review vol.53, pp.3, 2008, https://doi.org/10.1007/s12223-008-0024-z
  10. Rumen microbial (meta)genomics and its application to ruminant production vol.7, pp.suppl1, 2007, https://doi.org/10.1017/s1751731112000419
  11. Presence and Role of Anaerobic Hydrolytic Microbes in Conversion of Lignocellulosic Biomass for Biogas Production vol.45, pp.23, 2007, https://doi.org/10.1080/10643389.2015.1053727
  12. Isolation and Characterization of Potential Cellulose Degrading Bacteria from Sheep Rumen vol.13, pp.3, 2019, https://doi.org/10.22207/jpam.13.3.60
  13. Imaging Study by Mass Spectrometry of the Spatial Variation of Cellulose and Hemicellulose Structures in Corn Stalks vol.68, pp.13, 2007, https://doi.org/10.1021/acs.jafc.9b07579
  14. Influence of host genetics in shaping the rumen bacterial community in beef cattle vol.10, pp.1, 2020, https://doi.org/10.1038/s41598-020-72011-9