The Lachnospiraceae and Ruminococcaceae are two of the most abundant families from the order Clostridiales found in the mammalian gut environment, and have been associated with the maintenance of gut health. While they are both diverse groups, they share a common role as active plant degraders. By comparing the genomes of the Lachnospiraceae and Ruminococcaceae with the Clostridiaceae, a more commonly free-living group, we identify key carbohydrate-active enzymes, sugar transport mechanisms, and metabolic pathways that distinguish these two commensal groups as specialists for the degradation of complex plant material.
References
[1]
Collins, M.D.; Lawson, P.A.; Willems, A.; Cordoba, J.J.; Fernandez-Garayzabal, J.; Garcia, P.; Cai, J.; Hippe, H.; Farrow, J.A.E. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int. J. Syst. Bacteriol. 1994, 44, 812–826, doi:10.1099/00207713-44-4-812.
[2]
Stackebrandt, E.; Rainey, F.A. Phylogenic relationships. In The Clostridia: Molecular Biology and Pathogenesis; Rood, J.I., McClane, B.A., Songer, J.G., Titball, R.W., Eds.; Academic Press: New York, NY, USA, 1997.
[3]
Garrity, G.M.; Bell, J.A.; Lilburn, T. The Proteobacteria, Part A, Introductory Essays: The Revised Road Map to the Manual. In Bergey’s Manual? of Systematic Bacteriology; Brenner, D.J., Krieg, N.R., Staley, J.T., Garrity, G.M., Eds.; Springer: New York, NY, USA, 2005.
[4]
Ludwig, W.; Schleifer, K.-H.; Whitman, W.B. Revised road map to the phylum Firmicutes. In Bergey’s Manual? of Systematic Bacteriology; Vos, P., Garrity, G.M., Jones, D., Krieg, N.R., Ludwig, W., Rainey, F.A., Schleifer, K-H., Whitman, W.B., Eds.; Springer: New York, NY, USA, 2009.
[5]
De Long, E.F. The microbial ocean from genomes to biomes. Nature 2009, 459, 200–206, doi:10.1038/nature08059.
[6]
Jalanka-Tuovinen, J.; Salonen, A.; Nikkila, J.; Immonen, O.; Kekkonen, R.; Lahti, L.; Palva, A.; de Vos, W.M. Intestinal Microbiota in Healthy Adults: Temporal Analysis Reveals Individual and Common Core and Relation to Intestinal Symptoms. PLoS One 2011, 6, e23035, doi:10.1371/journal.pone.0023035.
[7]
Turnbaugh, P.J.; Hamady, M.; Yatsunenko, T.; Cantarel, B.L.; Duncan, A.; Ley, R.E.; Sogin, M.L.; Jones, W.J.; Roe, B.A.; Affourtit, J.P. A core gut microbiome in obese and lean twins. Nature 2008, 457, 480–484.
[8]
Peris-Bondia, F.; Latorre, A.; Artacho, A.; Moya, A.; D’Auria, G. The Active Human Gut Microbiota Differs from the Total Microbiota. PLoS One 2011, 6, e22448.
[9]
Tap, J.; Mondot, S.; Levenez, F.; Pelletier, E.; Caron, C.; Furet, J.; Ugarte, E.; Mu?oz-Tamayo, R.; Paslier, D.L.E; Nalin, R. Towards the human intestinal microbiota phylogenetic core. Environ. Microbiol. 2009, 11, 2574–2584, doi:10.1111/j.1462-2920.2009.01982.x.
[10]
Barcenilla, A.; Pryde, S.E.; Martin, J.C.; Duncan, S.H.; Stewart, C.S.; Henderson, C.; Flint, H.J. Phylogenetic Relationships of Butyrate-Producing Bacteria from the Human Gut. Appl. Environ. Microbiol. 2000, 66, 1654–1661, doi:10.1128/AEM.66.4.1654-1661.2000.
[11]
Duncan, S.H.; Barcenilla, A.; Stewart, C.S.; Pryde, S.E.; Flint, H.J. Acetate utilization and butyryl coenzyme A (CoA): acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Appl. Environ. Microbiol. 2002, 68, 5186–5190, doi:10.1128/AEM.68.10.5186-5190.2002.
[12]
Frank, D.N.; Amand, A.L.S.; Feldman, R.A.; Boedeker, E.C.; Harpaz, N.; Pace, N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 2007, 104, 13780–13785.
[13]
Flint, H.J.; Bayer, E.A.; Rincon, M.T.; Lamed, R.; White, B.A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 2008, 6, 121–131, doi:10.1038/nrmicro1817.
Fujimoto, T.; Imaeda, H.; Takahashi, K.; Kasumi, E.; Bamba, S.; Fujiyama, Y.; Andoh, A. Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn’s disease. J. Gastroen. Hepatol. 2013, 28, 613–619, doi:10.1111/jgh.12073.
[16]
Leschine, S. Cellulose Degradation in Anaerobic Environments. Annu. Rev. Microbiol. 1995, 49, 399–426, doi:10.1146/annurev.mi.49.100195.002151.
Brulc, J.M.; Antonopoulosb, D.A.; Millera, M.E.B.; Wilsona, M.K.; Yannarella, A.C.; Dinsdaled, E.A.; Edwardsd, R.E.; Frankh, E.D.; Emersoni, J.B.; Wacklini, P.; et al. Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl. Acad. Sci. USA 2009, 106, 1948–1953, doi:10.1073/pnas.0806191105.
[19]
Macfarlane, S.; Macfarlane, G.T. Composition and Metabolic Activities of Bacterial Biofilms Colonizing Food Residues in the Human Gut. Appl. Environ. Microbiol. 2006, 72, 6204–6211, doi:10.1128/AEM.00754-06.
Proctor, L.M. The Human Microbiome Project in 2011 and Beyond. Cell Host Microbe 2011, 10, 287–291, doi:10.1016/j.chom.2011.10.001.
[22]
Cole, J.R. The Ribosomal Database Project (RDP-II): Sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res. 2004, 33, D294–D296, doi:10.1093/nar/gki038.
[23]
Edgar, R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797, doi:10.1093/nar/gkh340.
[24]
Tamura, K.; Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10, 512–526.
[25]
Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol. Biol. Evol. 2011, 28, 2731–2739, doi:10.1093/molbev/msr121.
[26]
FigTreeversion 1.3.1. Available online: http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 17 May 2013).
[27]
Markowitz, V.M.; Chen, I.M.A.; Palaniappan, K.; Chu, K.; Szeto, E.; Gretchkin, Y. IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res. 2011, 40, D115–D122.
[28]
Cantarel, B.L.; Coutinho, P.M.; Rancurel, C.; Bernard, T.; Lombard, V.; Henrissat, B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009, 37, D233–D238, doi:10.1093/nar/gkn663.
[29]
R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2012. Version 2.15.1..
[30]
Venables, W.N.; Ripley, B.D. Modern Applied Statistics with S. Available online: http://www.stats.ox.ac.uk/pub/MASS4 (accessed on 17 May 2013).
[31]
Shapiro, S.S.; Wilk, M.B. An analysis of variance test for normality (complete samples). Biometrika 1965, 52, 591–611.
[32]
O’Hara, R.B.; Kotze, D.J. Do not log-transform count data. Methods Ecol. Evol. 2010, 1, 118–122, doi:10.1111/j.2041-210X.2010.00021.x.
[33]
The UniProt Consortium. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2011, 40, D71–D75, doi:10.1093/nar/gkr981.
[34]
Kanehisa, M.; Goto, S.; Sato, Y.; Furumichi, M.; Tanabe, M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2011, 40, D109–D114.
[35]
Keseler, I.M.; Mackie, A.; Peralta-Gil, M.; Santos-Zavaleta, A.; Gama-Castro, S.; Bonavides-Martinez, C.; Fulcher, C.; Huerta, A.M.; Kothari, A.; Krummenacker, M. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res. 2012, 41, D605–D612.
[36]
Karp, P.D. Expansion of the BioCyc collection of pathway/genome databases to 160 genomes. Nucleic Acids Res. 2005, 33, 6083–6089, doi:10.1093/nar/gki892.
[37]
Saier, M.H. Families of transmembrane sugar transport proteins. Mol. Microbiol. 2000, 35, 699–710, doi:10.1046/j.1365-2958.2000.01759.x.
[38]
Brückner, R.; Titgemeyer, F. Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol. Lett. 2002, 209, 141–148, doi:10.1111/j.1574-6968.2002.tb11123.x.
[39]
Jojima, T.; Omumasaba, C.A.; Inui, M.; Yukawa, H. Sugar transporters in efficient utilization of mixed sugar substrates: current knowledge and outlook. Appl. Microbiol. Biotechnol. 2009, 85, 471–480.
[40]
Stülke, J.; Hillen, W. Regulation of carbon catabolism in Bacillus species. Annu. Rev. Microbiol. 2000, 54, 849–880, doi:10.1146/annurev.micro.54.1.849.
[41]
Rees, D.C.; Johnson, E.; Lewinson, O. ABC transporters: the power to change. Nat. Rev. Mol. Cell Biol. 2009, 10, 218–227, doi:10.1038/nrm2646.