Production of butyrate from lysine and the Amadori product fructoselysine by a human gut commensal

Nature Communications

Volumn 6, Issue , 2015, Pages

  Bui, Thi Phuong Nam ^a   Ritari, Jarmo ^b   Boeren, Sjef ^a   De Waard, Pieter ^a   Plugge, Caroline M ^a   De Vos, Willem M ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; BUTYRIC ACID; COENZYME A TRANSFERASE; FRUCTOSELYSINE; LYSINE; LYSINE DERIVATIVE; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; UNCLASSIFIED DRUG; ACETIC ACID DERIVATIVE; BUTYRIC ACID DERIVATIVE; FRUCTOSAMINE; FRUCTOSYL-LYSINE;

AMINO ACID; BACTERIUM; CELLS AND CELL COMPONENTS; CHEMICAL REACTION; COMMENSAL; DIGESTIVE SYSTEM; ENZYME ACTIVITY; HOMINID; ORGANIC ACID; PROTEIN;

AMADORI REARRANGEMENT; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM; BACTERIUM CULTURE; BACTERIUM ISOLATION; COLON FLORA; COMMENSAL; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME SPECIFICITY; GENETIC CODE; GLYCATION; INTESTINE FLORA; INTESTINIMONAS BUTYRICIPRODUCENS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANISMS BY METABOLISM; SIGNAL TRANSDUCTION; STOICHIOMETRY; ADULT; ANALOGS AND DERIVATIVES; BIOTRANSFORMATION; CLOSTRIDIALES; COLON; FECES; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYLOGENY;

BACTERIA (MICROORGANISMS);

ACETATES; ADULT; BIOTRANSFORMATION; BUTYRATES; CLOSTRIDIALES; COLON; FECES; FRUCTOSAMINE; HUMANS; LYSINE; PHYLOGENY;

EID: 84948845104     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10062     Document Type: Article

References (53)

1. Sommer, F., Bäckhed, F. The gut microbiota-masters of host development and physiology. Nat. Rev. Microbiol. 11, 227-238 (2013).
2. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65 (2010).
3. Hamer, H. M. et al. Review article: the role of butyrate on colonic function. Aliment. Pharmacol. Ther. 27, 104-119 (2008).
4. Rajilić-Stojanović, M., de Vos, W. M. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol. Rev. 38, 996-1047 (2014).
5. Flint, H. J., Scott, K. P., Ducan, S., Louis, P., Forano, E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3, 289-306 (2012).
6. Qin, J. et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 55-60 (2012).
7. Scheppach, W., Luehrs, H., Menzel, T. Beneficial health effects of lowdigestible carbohydrate consumption. Br. J. Nutr. 85, S23-S30 (2001).
8. 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 butyrateproducing bacteria from the human large intestine. Appl. Environ. Microbiol. 68, 5186-5190 (2002).
9. Belenguer, A. et al. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl. Environ. Microbiol. 72, 3593-3599 (2006).
10. Barcenilla, A. et al. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl. Environ. Microbiol. 66, 1654-1661 (2000).
11. Louis, P., Hold, G. L., Flint, H. J. The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 12, 661-672 (2014).
12. Louis, P. et al. Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J. Bacteriol. 186, 2099-2106 (2004).
13. Vital, M., Howe, A. C., Tiedje, J. M. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. MBio 5, e00889 (2014).
14. Deppe, V., Bongaerts, J., O'Connell, T., Maurer, K. H., Meinhardt, F. Enzymatic deglycation of Amadori products in bacteria: mechanisms, occurrence and physiological functions. Appl. Microbiol. Biotechnol. 90, 399-406 (2011).
15. Stadtman, T. C., White, F. H. Tracer studies on ornithine, lysine, and formate metabolism in an amino acid fermenting clostridium. J. Bacteriol. 67, 651-657 (1954).
16. Kreimeyer, A. et al. Identification of the last unknown genes in the fermentation pathway of lysine. J. Biol. Chem. 282, 7191-7197 (2007).
17. Yorifuji, T., Jeng, I. M., Barker, H. A. Purification and properties of 3-keto-5-aminohexanoate cleavage enzyme from a lysine-fermenting clostridium. J. Biol. Chem. 252, 20-31 (1977).
18. Baker, J. J., Jeng, I., Barker, H. A. Purification and properties of l-erythro-3,5-diaminohexanoate dehydrogenase from a lysine-fermenting clostridium. J. Biol. Chem. 247, 7724-7734 (1972).
19. Barker, H. A. et al. Butyryl-CoA:acetoacetate CoA-transferase from a lysinefermenting clostridium. J. Biol. Chem. 253, 1219-1225 (1978).
20. Chirpich, T. P., Zappia, V., Costilow, R. N., Barker, H. A. Lysine 2,3-aminomutase: purification and properties of a pyridoxal phosphate and S-adenosylmethionine-activated enzyme. J. Biol. Chem. 245, 1778-1789 (1970).
21. Kläring, K. et al. Intestinimonas butyriciproducens gen. nov., sp. nov., a butyrate-producing bacterium from the mouse intestine. Int. J. Syst. Evol. Microbiol. 63, 4606-4612 (2013).
22. Wiame, E., Van Schaftingen, E. Fructoselysine 3-epimerase, an enzyme involved in the metabolism of the unusual Amadori compound psicoselysine in Escherichia coli. Biochem. J. 378, 1047-1052 (2004).
23. Wiame, E., Delpierre, G., Collard, F., Van Schaftingen, E. Identification of a pathway for the utilization of the Amadori product fructoselysine in Escherichia coli. J. Biol. Chem. 277, 42523-42529 (2002).
24. Plugge, C. M., van Leeuwen, J., Hummelen, T., Balk, M., Stams, A. J. M. Elucidation of the pathways of catabolic glutamate conversion in three thermophilic anaerobic bacteria. Arch. Microbiol. 176, 29-36 (2001).
25. Herrmann, G., Jayamani, E., Mai, G., Buckel, W. Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J. Bacteriol. 190, 784-791 (2008).
26. Li, F. et al. Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J. Bacteriol. 190, 843-850 (2008).
27. Boynton, Z. L., Bennet, G. N., Rudolph, F. B. Cloning, sequencing, and expression of clustered genes encoding beta-hydroxybutyryl-coenzyme A (CoA) dehydrogenase, crotonase, and butyryl-CoA dehydrogenase from Clostridium acetobutylicum ATCC 824. J. Bacteriol. 178, 3015-3024 (1996).
28. Charrier, C. et al. A novel class of CoA-transferase involved in short-chain fatty acid metabolism in butyrate-producing human colonic bacteria. Microbiology 152, 179-185 (2006).
29. Fonknechten, N. et al. Clostridium sticklandii, a specialist in amino acid degradation:revisiting its metabolism through its genome sequence. BMC Genomics 11, 1-12 (2010).
30. Wiesenborn, D. P., Rudolph, F. B., Papoutsakis, E. T. Coenzyme A transferase from Clostridium acetobutylicum ATCC 824 and its role in the uptake of acids. Appl. Environ. Microbiol. 55, 323-329 (1989).
31. Bennett, G. N., Rudolph, F. B. The central metabolic pathway from acetyl-CoA to butyryl-CoA in Clostridium acetobutylicum. FEMS Microbiol. Rev. 17, 241-249 (1995).
32. Barker, H. A., Kahn, J. M., Hedrick, L. Pathway of lysine degradation in Fusobacterium nucleatum. J. Bacteriol. 152, 201-207 (1982).
33. Kapatral, V. et al. Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J. Bacteriol. 184, 2005-2018 (2002).
34. Bui, T. P. N., de Vos, W. M., Plugge, C. M. Anaerostipes rhamnosivorans sp. nov., a human intestinal, butyrate-forming bacterium. Int. J. Syst. Evol. Microbiol. 64, 787-793 (2014).
35. The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214 (2012).
36. Rettedal, E. A., Gumpert, H., Sommer, M. O. A. Cultivation-based multiplex phenotyping of human gut microbiota allows targeted recovery of previously uncultured bacteria. Nat. Commun. 5, 4714 (2014).
37. Leiros, H. K. et al. Trypsin specificity as elucidated by LIE calculations, X-ray structures, and association constant measurements. Protein Sci. 13, 1056-1070 (2004).
38. Rogers, A. H., Chen, J., Zilm, P. S., Gully, N. J. The behaviour of Fusobacterium nucleatum chemostat-grown in glucose-and amino acid-based chemically defined media. Anaerobe 4, 111-116 (1998).
39. Windey, K. et al. Modulation of protein fermentation does not affect fecal water toxicity: a randomized cross-over study in healthy subjects. PLoS ONE 7, e52387 (2012).
40. Brownlee, M. Glycation and diabetic complications. Diabetes 43, 836-841 (1994).
41. Baynes, J. W., Thorpe, S. R. Glycoxidation and lipoxidation in atherogenesis. Free Radic. Biol. Med. 28, 1708-1716 (2000).
42. West, R. K. et al. Dietary advanced glycation end products are associated with decline in memory in young elderly. Mech. Ageing Dev. 140, 10-12 (2014).
43. Cai, W. et al. Oral glycotoxins are a modifiable cause of dementia and the metabolic syndrome in mice and humans. Proc. Natl Acad. Sci. USA 111, 4940-4945 (2014).
44. Stams, A. J. M., Van Dijk, J. B., Dijkema, C., Plugge, C. M. Growth of syntrophic propionate-oxidizing bacteria with fumarate in the absence of methanogenic bacteria. Appl. Environ. Microbiol. 59, 1114-1119 (1993).
45. Zwietering, M. H., Jongenburger, I., Rombouts, F. M., Van 't Riet, K. Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56, 1875-1881 (1990).
46. van Gelder, A. H., Aydin, R., Alves, M. M., Stams, A. J. M. 1,3-Propanediol production from glycerol by a newly isolated Trichococcus strain. Microbiol. Biotechnol. 5, 573-578 (2012).
47. Oosterkamp, M. J., Boeren, S., Plugge, C. M., Schaap, P. J., Stams, A. J. M. Metabolic response of Alicycliphilus denitrificans strain BC toward electron acceptor variation. Proteomics 13, 2886-2894 (2013).
48. Louis, P., Flint, H. J. Diversity, metabolism and microbial ecology of butyrateproducing bacteria from the human large intestine. FEMS Microbiol. Lett. 294, 1-8 (2009).
49. Gerischer, U., Dürre, P. Cloning, sequencing, and molecular analysis of the acetoacetate decarboxylase gene region from Clostridium acetobutylicum. J. Bacteriol. 172, 6907-6918 (1990).
50. Salonen, A. et al. Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: Effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J. Microbiol. Methods 81, 127-134 (2010).
51. Walter, J. et al. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 67, 2578-2585 (2001).
52. Suzuki, M. T., Taylor, L. T., DeLong, E. F. Quantitative analysis of smallsubunit rRNA genes in mixed microbial populations via 50-nuclease assays. Appl. Environ. Microbiol. 66, 4605-4614 (2000).
53. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).