The complete genome sequence of fibrobacter succinogenes s85 reveals a cellulolytic and metabolic specialist

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Suen, Garret ^a   Weimer, Paul J ^b   Stevenson, David M ^b   Aylward, Frank O ^a   Boyum, Julie ^c   Deneke, Jan ^c   Drinkwater, Colleen ^c   Ivanova, Natalia N ^d   Mikhailova, Natalia ^d   Chertkov, Olga ^e   Goodwin, Lynne A ^d,e   Currie, Cameron R ^a   Mead, David ^a,c   Brumm, Phillip J ^a,f  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b U S DAIRY FORAGE RESEARCH CENTER   (United States)

^c LUCIGEN CORPORATION   (United States)

^d DOE JOINT GENOME INSTITUTE   (United States)

^e LOS ALAMOS NATIONAL LABORATORY   (United States)

^f C5 6 Technologies   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CARBOHYDRATE BINDING MODULE; CARBOHYDRATE DEGRADING ENZYME; CARBOHYDRATE ESTERASE; CELLULASE; CELLULOSE; GLYCOSIDASE; HEMICELLULOSE; POLYSACCHARIDE LYASE; UNCLASSIFIED DRUG; BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; ESTERASE; HEMICELLULASE; PROTEOME;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; CARBOHYDRATE METABOLISM; FIBROBACTER SUCCINOGENES; GENE SEQUENCE; HYDROLYSIS; NONHUMAN; OPEN READING FRAME; ANIMAL; BACTERIUM ADHERENCE; BIOCATALYSIS; CLASSIFICATION; ENZYMOLOGY; FIBROBACTER; GENETICS; METABOLISM; MICROBIOLOGY; PHYLOGENY; RUMINANT STOMACH; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIA (MICROORGANISMS); FIBROBACTER SUCCINOGENES;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOCATALYSIS; BIOLOGICAL TRANSPORT; CELLULASE; CELLULOSE; ESTERASES; FIBROBACTER; GENES, BACTERIAL; GENOME, BACTERIAL; GLYCOSIDE HYDROLASES; HYDROLYSIS; PHYLOGENY; POLYSACCHARIDES, BACTERIAL; PROTEOME; RUMEN;

EID: 79955446915     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018814     Document Type: Article

References (98)

1. Russell JB, (2002) Rumen microbiology and its role in ruminant nutrition. Ithaca, NY J.B. Russell Publishing Co.
2. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA, (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Micro 6: 121-131.
3. Hungate RE, (1950) The anaerobic mesophilic cellulolytic bacteria. Bacteriol Rev 14: 1-49.
4. Montgomery L, Flesher B, Stahl D, (1988) Transfer of Bacteroides succinogenes (Hungate) to Fibrobacter gen. nov. as Fibrobacter succinogenes comb. nov. and Description of Fibrobacter intestinalis sp. nov. Int J Syst Evol Microbiol 38: 430-435.
5. Stevenson DM, Weimer PJ, (2007) Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl Microbiol Biotechnol 75: 165-174.
6. Kobayashi Y, Shinkai T, Koike S, (2008) Ecological and physiological characterization shows that Fibrobacter succinogenes is important in rumen fiber digestion - Review. Folia Microbiol 53: 195-200.
7. Weimer PJ, (1993) Effects of dilution rate and pH on the ruminal cellulolytic bacterium Fibrobacter succinogenes S85 in cellulose-fed continuous culture. Archives of Microbiology 160: 288-294.
8. Russell JB, (1985) Fermentation of cellodextrins by cellulolytic and noncellulolytic rumen bacteria. Appl Environ Microbiol 49: 572-576.
9. Shi Y, Weimer PJ, (1996) Utilization of individual cellodextrins by three predominant ruminal cellulolytic bacteria. Appl Environ Microbiol 62: 1084-1088.
10. Wells JE, Russell JB, Shi Y, Weimer PJ, (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.
11. Doi RH, Kosugi A, (2004) Cellulosomes: plant-cell-wall-degrading enzyme complexes. Nat Rev Micro 2: 541-551.
12. Bayer EA, Belaich J-P, Shoham Y, Lamed R, (2004) The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol 58: 521-554.
13. Kudo H, Cheng KJ, Costerton JW, (1987) Electron microscopic study of the methylcellulose-mediated detachment of cellulolytic rumen bacteria from cellulose fibers. Can J Microbiol 33: 267-272.
14. Weimer PJ, Odt CL, (1996) Cellulose degradation by ruminal microbes: physiological and hydrolytic diversity among ruminal cellulolytic bacteria. In: Saddler J, Penner M, editors. Enzymatic Degradation of Insoluble Carbohydrates Washington, DC American Chemical Society pp. 291-304.
15. Ogata K, Aminov RI, Nagamine T, Sugiura M, Tajima K, et al. (1997) Construction of a Fibrobacter succinogenes Genomic map and demonstration of diversity at the genomic level. Curr Microbiol 35: 22-27.
16. Gupta RS, (2004) The phylogeny and signature sequences characteristics of Fibrobacteres, Chlorobi, and Bacteroidetes. Crit Rev Microbiol 30: 123-143.
17. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, et al. (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311: 1283-1287.
18. Griffiths E, Gupta RS, (2001) The use of signature sequences in different proteins to determine the relative branching order of bacterial divisions: evidence that Fibrobacter diverged at a similar time to Chlamydia and the Cytophaga-Flavobacterium-Bacteroides division. Microbiology 147: 2611-2622.
19. Koonin EV, Wolf YI, (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36: 6688-6719.
20. Tatusov RL, Galperin MY, Natale DA, Koonin EV, (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28: 33-36.
21. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37: D233-238.
22. Brumm P, Mead D, Boyum J, Drinkwater C, Gowda K, et al. (2010) Functional annotation of Fibrobacter succinogenes S85 carbohydrate active enzymes. Appl Biochem Biotechnol 10.1007/s12010-12010-19070-12015.
23. Iyo AH, Forsberg CW, (1994) Features of the cellodextrinase gene from Fibrobacter succinogenes S85. Can J Microbiol 40: 592-596.
24. Iyo AH, Forsberg CW, (1996) Endoglucanase G from Fibrobacter succinogenes S85 belongs to a class of enzymes characterized by a basic C-terminal domain. Can J Microbiol 42: 934-943.
25. Broussolle V, Forano E, Gaudet G, Ribot Y, (1994) Gene sequence and analysis of protein domains of EGB, a novel family E endoglucanase from Fibrobacter succinogenes S85. FEMS Microbiol Lett 124: 439-447.
26. McGavin MJ, Forsberg CW, Crosby B, Bell AW, Dignard D, et al. (1989) Structure of the cel-3 gene from Fibrobacter succinogenes S85 and characteristics of the encoded gene product, endoglucanase 3. J Bacteriol 171: 5587-5595.
27. Qi M, Jun H-S, Forsberg CW, (2007) Characterization and synergistic interactions of Fibrobacter succinogenes glycoside hydrolases. Appl Environ Microbiol 73: 6098-6105.
28. Malburg LM Jr, Iyo AH, Forsberg CW, (1996) A novel family 9 endoglucanase gene (celD), whose product cleaves substrates mainly to glucose, and its adjacent upstream homolog (celE) from Fibrobacter succinogenes S85. Appl Environ Microbiol 62: 898-606.
29. Qi M, Jun H-S, Forsberg CW, (2008) Cel9D, an atypical 1,4-β-D-glucan glucohydrolase from Fibrobacter succinogenes: characteristics, catalytic residues, and synergistic interactions with other cellulases. J Bacteriol 190: 1976-1984.
30. Cavicchioli R, Watson K, (1991) Molecular cloning, expression, and characterization of endoglucanase genes from Fibrobacter succinogenes AR1. Appl Environ Microbiol 57: 359-365.
31. 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.
32. Jun H-S, Ha JK, Malburg LM Jr, Verrinder GA, Forsberg CW, (2003) Characteristics of a cluster of xylanase genes in Fibrobacter succinogenes S85. Can J Microbiol 49: 171-180.
33. Jun H-S, 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.
34. Paradis FW, Zhu H, Krell PJ, Phillips JP, Forsberg CW, (1993) The xynC gene from Fibrobacter succinogenes S85 codes for a xylanase with two similar catalytic domains. J Bacteriol 175: 7666-7672.
35. Mitsumori M, Minato H, Sekizaki T, Uchida I, Ito H, (1996) Cloning, nucleotide sequence and expression of the gene encoding the cellulose-binding protein 1 (CBP1) of Fibrobacter succinogenes S85. FEMS Microbiol Lett 139: 43-50.
36. Kam DK, Jun H-S, Ha JK, Inglis GD, Forsberg CW, (2005) Characteristics of adjacent family 6 acetylxylan esterases from Fibrobacter succinogenes and the interaction with the Xyn10E xylanase in hydrolysis of acetylated xylan. Can J Microbiol 51: 821-883.
37. Teather RM, Erfle JD, (1990) DNA sequence of a Fibrobacter succinogenes mixed-linkage beta-glucanase (1,3-1,4-beta-D-glucan 4-glucanohydrolase) gene. J Bacteriol 172: 3837-3841.
38. Cho KK, Kim SC, Woo JH, Bok JD, Choi YJ, (2000) Molecular cloning and expression of a novel family A endoglucanase gene from Fibrobacter succinogenes S85 in Escherichia coli. Enzyme Microb Technol 27: 475-481.
39. Emanuelsson O, Brunak S, von Heijne G, Nielsen H, (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protocols 2: 953-971.
40. Groleau D, Forsberg CW, (1981) Cellulolytic activity of the rumen bacterium Bacteroides succinogenes. Can J Microbiol 27: 517-530.
41. Yoshida S, Hespen CW, Beverly RL, Mackie RI, Cann IKO, (2010) Domain analysis of a modular alpha-L-arabinofuranosidase with a unique carbohydrate binding strategy from the fiber degrading bacterium Fibrobacter succinogenes S85. J Bacteriol doi:10.1128/JB.00503-00510.
42. Tamaru Y, Karita S, Ibrahim A, Chan H, Doi RH, (2000) A large gene cluster for the Clostridium cellulovorans cellulosome. J Bacteriol 182: 5906-5910.
43. Han SO, Yukawa H, Inui M, Doi RH, (2003) Transcription of Clostridium cellulovorans cellulosomal cellulase and hemicellulase genes. J Bacteriol 185: 2520-2527.
44. Spiridonov NA, Wilson DB, (1999) Characterization and cloning of celR, a transcriptional regulator of cellulase genes from Thermomonospora fusca. J Biol Chem 274: 13127-13132.
45. Centeno MS, Goyal A, Prates JA, Ferreira LM, Gilbert HJ, et al. (2006) Novel modular enzymes encoded by a cellulase gene cluster in Cellvibrio mixtus. FEMS Microbiol Lett 265: 26-34.
46. Yoshida S, Mackie RI, Cann IKO, (2010) Biochemical and domain analyses of FSUAxe6B, a modular acetyl xylan esterase, identify a unique carbohydrate binding module in Fibrobacter succinogenes S85. J Bacteriol 192: 483-493.
47. McDermid KP, Forsberg CW, MacKenzie CR, (1990) Purification and properties of an acetylxylan esterase from Fibrobacter succinogenes S85. Appl Environ Microbiol 56: 3805-3810.
48. Kam DK, Jun HS, Ha JK, Inglis GD, Forsberg CW, (2005) Characteristics of adjacent family 6 acetylxylan esterases from Fibrobacter succinogenes and the interaction with the Xyn10E xylanase in hydrolysis of acetylated xylan. Can J Microbiol 51: 821-832.
49. Yoshida S, Mackie RI, Cann IKO, (2009) Biochemical and Domain Analyses of FSUAxe6B, a Modular Acetyl Xylan Esterase, Identify a Unique Carbohydrate Binding Module in Fibrobacter succinogenes S85. Journal of Bacteriology 192: 483-493.
50. Gong J, Egbosimba EE, Forsberg CW, (1996) Cellulose-binding proteins of Fibrobacter succinogenes and the possible role of a 180-kDa cellulose-binding glycoprotein in adhesion to cellulose. Can J Microbiol 42: 453-460.
51. Moreira CG, Palmer K, Whiteley M, Sircili MP, Trabulsi LR, et al. (2006) Bundle-forming pili and EspA are involved in biofilm formation by enteropathogenic Escherichia coli. J Bacteriol 188: 3952-3961.
52. Cianciotto NP, (2005) Type II secretion: a protein secretion system for all seasons. Trends in Microbiol 13: 581-588.
53. Nataf Y, Yaron S, Stahl F, Lamed R, Bayer EA, et al. (2009) Cellodextrin and laminaribiose ABC transporters in Clostridium thermocellum. J Bacteriol 191: 203-209.
54. Alexander JK, (1961) Characteristics of cellobiose phosphorylase. J Bacteriol 81: 903-910.
55. Alexander JK, Victor G, (1972) Cellobiose phosphorylase from Clostridium thermocellum. Methods Enzymol 130: 944-948.
56. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS, (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66: 506-577.
57. Huang L, McGavin M, Forsberg CW, Lam JS, Cheng KJ, (1990) Antigenic nature of the chloride-stimulated cellobiosidase and other cellulases of Fibrobacter succinogenes subsp. succinogenes S85 and related fresh isolates. Appl Environ Microbiol 56: 1229-1234.
58. Claudel-Renard C, Chevalet C, Faraut T, Kahn D, (2003) Enzyme-specific profiles for genome annotation: PRIAM. Nucleic Acids Res 31: 6633-6639.
59. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M, (2009) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38: D355-D360.
60. Miller TL, (1978) The pathway of formation of acetate and succinate from pyruvate by Bacteroides succinogenes. Arch Microbiol 117: 145-152.
61. Asanuma N, Hino T, (2000) Activity and properties of fumarate reductase in ruminal bacteria. J Gen Appl Microbiol 46: 119-125.
62. Vignais PM, Billoud B, (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107: 4206-4272.
63. Kelly WJ, Leahy SC, Altermann E, Yeoman CJ, Dunne JC, et al. (2010) The glycobiome of the rumen bacterium Butyrivibrio proteoclasticus B316 highlights adaptation to a polysaccharide-rich environment. PLoS ONE 5: e11942.
64. Purushe J, Fouts D, Morrison M, White B, Mackie R, et al. (2010) Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol doi:10.1007/s00248-010-9692-8.
65. Berg Miller ME, Antonopoulos DA, Rincon MT, Band M, Bari A, et al. (2009) Diversity and strain specificity of plant cell wall degrading enzymes revealed by the draft genome of Ruminococcus flavefaciens FD-1. PLoS ONE 4: e6650.
66. Weimer PJ, French AD, Calamari TA Jr, (1991) Differential fermentation of cellulose allomorphs by ruminal cellulolytic bacteria. Appl Biochem Biotechnol 57: 3101-3106.
67. Ozcan N, Cunningham C, Harris W, (1996) Cloning of a cellulase gene from the rumen anaerobe Fibrobacter succinogenes SD35 and partial characterization of the gene product. Lett Appl Microbiol 22: 85-89.
68. Weimer PJ, (1996) Why don't ruminal bacteria digest cellulose faster? J Dairy Sci 79: 1496-1502.
69. Costerton WJ, (1992) Pivotal role of biofilms in the focused attack of bacteria on insoluble substrates. Int Biodet Biodeg 30: 123-133.
70. Jun H-S, Qi M, Ha JK, Forsberg CW, (2007) Fibrobacter succinogenes, a Dominant Fibrolytic Ruminal Bacterium: Transition to the Post Genomic Era. Asian-Aust J Anim Sci 20: 802-810.
71. Gong J, Forsberg CW, (1993) Separation of outer and cytoplasmic membranes of Fibrobacter succinogenes and membrane and glycogen granule locations of glycanases and cellobiase. J Bacteriol 175: 6810-6821.
72. Morrison M, Pope PB, Denman SE, McSweeney CS, (2009) Plant biomass degradation by gut microbiomes: more of the same or something new? Curr Opin Biotechnol 20: 358-363.
73. Wilson DB, (2009) Evidence for a novel mechanism of microbial cellulose degradation. Cellulose 16: 723-727.
74. Xie G, Bruce DC, Challacombe JF, Chertkov O, Detter JC, et al. (2007) Genome sequence of the cellulolytic gliding bacterium Cytophaga hutchinsonii. Appl Environ Microbiol 73: 3536-3546.
75. Hashimoto W, Momma K, Maruyama Y, Yamasaki M, Mikami B, et al. (2005) Structure and function of bacterial super-biosystem responsible for import and depolymerization of macromolecules. Biosci Biotechnol Biochem 69: 673-692.
76. Hashimoto W, He J, Wada Y, Nankai H, Mikami B, et al. (2005) Proteomics-based identification of outer-membrane proteins responsible for import of macromolecules in Sphingomonas sp. A1: alginate-binding flagellin on the cell surface. Biochemistry 44: 13783-13794.
77. Lin C, Stahl DA, (1995) Taxon-specific probes for the cellulolytic genus Fibrobacter reveal abundant and novel equine-associated populations. Appl Environ Microbiol 61: 1348-1351.
78. Matsui H, Kato Y, Chikaraishi T, Moritani M, Ban-Tokuda T, et al. (2010) Microbial diversity in ostrich ceca as revealed by 16S ribosomal RNA gene clone library and detection of novel Fibrobacter species. Anaerobe 16: 83-93.
79. Bennett S, (2004) Solexa Ltd. Pharmacogenomics 5: 433-438.
80. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
81. Zerbino DR, Birney E, (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
82. Ewing B, Green P, (1998) Base-calling of automated sequencer traces using Phred. II. error probabilities. Genome Res 8: 186-194.
83. Ewing B, Hillier L, Wendl MC, Green P, (1998) Base-calling of automated sequencer traces using Phred. I. accuracy assessment. Genome Res 8: 175-185.
84. Gordon D, Abajian C, Green P, (1998) Consed: a graphical tool for sequence finishing. Genome Res 8: 195-202.
85. Han CS, Chain P, (2006) Finishing repeat regions automatically with Dupfinisher. In: Arabnia HR, Valafar H, editors. Proceedings of the 2006 International Conference on Bioinformatics & Computational Biology: CSREA Press pp. 141-146.
86. Hyatt D, Chen G-L, LoCascio P, Land M, Larimer F, et al. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
87. Pati A, Ivanova NN, Mikhailova N, Ovchinnikova G, Hooper SD, et al. (2010) GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes. Nat Meth 7: 455-457.
88. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-D222.
89. The UniProt Consortium (2008) The Universal Protein Resource (UniProt). Nucleic Acids Res 36: D190-D195.
90. Haft DH, Selengut JD, White O, (2003) The TIGRFAMs database of protein families. Nucleic Acids Res 31: 371-373.
91. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: D211-D215.
92. Lowe T, Eddy SR, (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
93. Lagesen K, Hallin P, Rodland EA, Staerfeldt H-H, Rognes T, et al. (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: 3100-3108.
94. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
95. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. (2009) CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res 37: D205-D210.
96. Weimer PJ, Shi Y, Odt CL, (1991) A segmented gas/liquid delivery system for continuous culture of microorganisms on insoluble substrates and its use for growth of Ruminococcus flavefaciens on cellulose. Appl Environ Microbiol 36: 178-183.
97. Miller GL, Blum R, Glennon WE, Burton AL, (1960) Measurement of carboxymethylcellulase activity. Anal Biochem 1: 127-132.
98. Maglione G, Russell JB, (1997) The adverse effect of nitrogen limitation and excess-cellobiose on Fibrobacter succinogenes S85. Appl Microbiol Biotechnol 48: 720-725.