Proteomic investigation of amino acid catabolism in the indigenous gut anaerobe Fusobacterium varium

Proteomics

Volumn 8, Issue 13, 2008, Pages 2691-2703

  Potrykus, Joanna ^a   White, Robert L ^b   Bearne, Stephen L ^a,b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

2 DE amino acid fermentation; Fusobacterium varium; Tandem mass spectrometry

Indexed keywords

2 HYDROXYGLUTARYL COENZYME A DEHYDRATASE; ACETIC ACID; AMINO ACID; AMMONIA LYASE; ASPARTATE SEMIALDEHYDE DEHYDROGENASE; BETA METHYLASPARTATE AMMONIA LYASE; BUTYRIC ACID; COENZYME A; DEXTRO GLUTAMIC ACID; DEXTRO LYSINE; DEXTRO SERINE; DIAMINOPIMELIC ACID; DIHYDRODIPICOLINATE REDUCTASE; DIHYDRODIPICOLINATE SYNTHASE; GLUCOSE; GLUTAMATE DEHYDROGENASE; GLUTAMIC ACID; HISTIDINE; HYDROLYASE; MESO 2,6 DIAMINO PIMELIC ACID; METHYLASPARTATE MUTASE; MUTASE; PIMELIC ACID DERIVATIVE; SALICYLURIC ACID; SERINE; SYNTHETASE;

AMINO ACID ANALYSIS; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL FUNCTION; CONTROLLED STUDY; FERMENTATION TECHNIQUE; FUNCTIONAL PROTEOMICS; FUSOBACTERIUM VARIUM; INTESTINE FLORA; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; PROTEIN TRANSPORT;

AMINO ACIDS; BACTERIA, ANAEROBIC; FERMENTATION; FUSOBACTERIUM; HUMANS; INTESTINES; PROTEOME; PROTEOMICS; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); FUSOBACTERIUM VARIUM;

EID: 47249129081     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200700437     Document Type: Article

References (77)

1. Xu, J., Gordon, J. I., Honor thy symbionts. Proc. Natl. Acad. Sci. USA 2003, 100, 10452-10459.
2. Karlsson, H., Hessle, C., Rudin, A., Innate immune responses of human neonatal cells to bacteria from the normal gastrointestinal flora. Infect. Immun. 2002, 70, 6688-6696.
3. Pavan, S., Desreumaux, P., Mercenier, A., Use of mouse models to evaluate the persistence, safety, and immune modulation capacities of lactic acid bacteria. Clin. Diagn. Lab. Immunol. 2003, 10, 696-701.
4. Shin, R., Suzuki, M., Morishita, Y., Influence of intestinal anaerobes and organic acids on the growth of enterohaemorrhagic Escherichia coli O157:H7. J. Med. Microbiol. 2002, 51, 201-206.
5. Wilson, K. H., Perini, F., Role of competition for nutrients in suppression of Clostridium difficile by the colonic microflora. Infect. Immun. 1988, 56, 2610-2614.
6. Guarner, F., Malagelada, J. R., Gut flora in health and disease. Lancet 2003, 361, 512-519.
7. Metges, C. C., Contribution of microbial amino acids to amino acid homeostasis of the host. J. Nutr. 2000, 130, 1857S-1864S.
8. Cummings, J. H., Macfarlane, G. T., The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol. 1991, 70, 443-459.
9. McGarr, S. E., Ridlon, J. M., Hylemon, P. B., Diet, anaerobic bacterial metabolism, and colon cancer: A review of the literature. J. Clin. Gastroenterol. 2005, 39, 98-109.
10. Noack, J., Dongowski, G., Hartmann, L., Blaut, M., The human gut bacteria Bacteroides thetaiotaomicron and Fusobacterium varium produce putrescine and spermidine in cecum of pectin-fed gnotobiotic rats. J. Nutr. 2000, 130, 1225-1231.
11. Smith, E. A., Macfarlane, G. T., Formation of phenolic and indolic compounds by anaerobic bacteria in the human large intestine. Microb. Ecol. 1997, 33, 180-188.
12. de Wiele, T. V., Boon, N., Possemiers, S., Jacobs, H., Verstraete, W., Prebiotic effects of chicory inulin in the simulator of the human intestinal microbial ecosystem. FEMS Microbiol. Ecol. 2004, 51, 143-153.
13. Walker, A. W., Duncan, S., McWilliam Leitch, E. C., Child, M. W., Flint, H. J., pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microbiol. 2005, 71, 3692-3700.
14. Pryde, S. E., Duncan, S. H., Hold, G. L., Stewart, C. S., Flint, H. J., The microbiology of butyrate formation in the human colon. FEMS Microbiol. Lett. 2002, 217, 133-139.
15. Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M. et al., The human microbiome project. Nature 2007, 449, 804-810.
16. Rolfe, R. D., The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 2000, 130, 396S-402S.
17. Ushijima, T., Ozaki, Y., Potent antagonism of Escherichia coli, Bacteroides ovatus, Fusobacterium varium, and Enterococcus faecalis, alone or in combination, for enteropathogens in anaerobic continuous flow cultures. J. Med. Microbiol. 1986, 22, 157-163.
18. Coleman, M. E., Dreesen, D. W., Wiegert, R. G., A simulation of microbial competition in the human colonic ecosystem. Appl. Environ. Microbiol. 1996, 62, 3632-3639.
19. Ushijima, T., Seto, A., Selected faecal bacteria and nutrients essential for antagonism of Salmonella typhimurium in anaerobic continuous flow cultures. J. Med. Microbiol. 1991, 35, 111-117.
20. Potrykus, J., Mahaney, B., White, R. L., Bearne, S. L., Proteomic investigation of glucose metabolism in the butyrate-producing gut anaerobe Fusobacterium varium. Proteomics 2007, 7, 1839-1853.
21. Macfarlane, G. T., Macfarlane, S., Human colonic microbiota: Ecology, physiology and metabolic potential of intestinal bacteria. Scand. J. Gastroenterol. Suppl. 1997, 222, 3-9.
22. George, W. L., Kirby, B. D., Sutter, V. L., Citron, D. M., Finegold, S. M., Gram-negative anaerobic bacilli: Their role in infection and patterns of susceptibility to antimicrobial agents. II. Little-known Fusobacterium species and miscellaneous genera. Rev. Infect. Dis. 1981, 3, 599-626.
23. Cummings, J. H., Pomare, E. W., Branch, W. J., Naylor, C. P., Macfarlane, G. T., Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 1987, 28, 1221-1227.
24. Di Sabatino, A., Morera, R., Ciccocioppo, R., Cazzola, P. et al., Oral butyrate for mildly to moderately active Crohn's disease. Aliment. Pharmacol. Ther. 2005, 22, 789-794.
25. Scheppach, W., Weiler, F., The butyrate story: Old wine in new bottles? Curr. Opin. Clin. Nutr. Metab. Care 2004, 7, 563-567.
26. Bolstad, A. I., Jensen, H. B., Bakken, V., Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clin. Microbiol. Rev. 1996, 9, 55-71.
27. Kolenbrander, P. E., London, J., Adhere today, here tomorrow: Oral bacterial adherence. J. Bacteriol. 1993, 175, 3247-3252.
28. Kamma, J. J., Nakou, M., Persson, R. G., Association of early onset periodontitis microbiota with aspartate aminotransferase activity in gingival crevicular fluid. J. Clin. Periodontol. 2001, 28, 1096-1105.
29. Ohkusa, T., Okayasu, I., Ogihara, T., Morita, K. et al., Induction of experimental ulcerative colitis by Fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis. Gut 2003, 52, 79-83.
30. Onderdonk, A. B., Bartlett, J. G., Louie, T., Sullivan-Seigler, N., Gorbach, S. L., Microbial synergy in experimental intraabdominal abscess. Infect. Immun. 1976, 13, 22-26.
31. Hong, F. U., Ying Qiang, S. H. I., Shan Jin, M. O., Effect of short-chain fatty acids on the proliferation and differentiation of the human colonic adenocarcinoma cell line Caco-2. Chin. J. Dig. Dis. 2004, 5, 115-117.
32. Williams, E. A., Coxhead, J. M., Mathers, J. C., Anti-cancer effects of butyrate: Use of micro-array technology to investigate mechanisms. Proc. Nutr. Soc. 2003, 62, 107-115.
33. Yuan, H., Liddle, F. J., Mahajan, S., Frank, D. A., IL-6-induced survival of colorectal carcinoma cells is inhibited by butyrate through down-regulation of the IL-6 receptor. Carcinogenesis 2004, 25, 2247-2255.
34. Bennett, K. W., Eley, A., Fusobacteria: New taxonomy and related diseases. J. Med. Microbiol. 1993, 39, 246-254.
35. Kapatral, V., Anderson, I., Ivanova, N., Reznik, G. et al., Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J. Bacteriol. 2002, 184, 2005-2018.
36. Kapatral, V., Ivanova, N., Anderson, I., Reznik, G. et al., Genome analysis of F. nucleatum sub spp vincentii and its comparison with the genome of F. nucleatum ATCC 25586. Genome Res. 2003, 13, 1180-1189.
37. Karpathy, S. E., Qin, X., Gioia, J., Jiang, H. et al., Genome sequence of Fusobacterium nucleatum subspecies polymorphum - a genetically tractable fusobacterium. PLoS ONE 2007, 2, e659.
38. Zilm, P. S., Rogers, A. H., Co-adhesion and biofilm formation by Fusobacterium nucleatum in response to growth pH. Anaerobe 2007, 13, 146-152.
39. Gharbia, S. E., Shah, H. N., Characteristics of glutamate dehydrogenase, a new diagnostic marker for the genus Fusobacterium. J. Gen. Microbiol 1988, 134, 327-332.
40. Gharbia, S. E., Shah, H. N., Identification of Fusobacterium species by the electrophoretic migration of glutamate dehydrogenase and 2-oxoglutarate reductase in relation to their DNA base composition and peptidoglycan dibasic amino acids. J. Med. Microbiol. 1990, 33, 183-188.
41. Morris, M. L., Andrews, R. H., Rogers, A. H., The use of allozyme electrophoresis to assess genetic heterogeneity among previously subspeciated isolates of Fusobacterium nucleatum. Oral Microbiol. Immunol. 1996, 11, 15-21.
42. Citron, D. M., Update on the taxonomy and clinical aspects of the genus Fusobacterium. Clin. Infect. Dis. 2002, 35, S22-S27.
43. Kim, H. J., Lee, D. Y., Lee, D. H., Park, Y. C. et al., Strategic proteome analysis of Candida magnoliae with an unsequenced genome. Proteomics 2004, 4, 3588-3599.
44. Kim, E. A., Kim, J. Y., Kim, S. J., Park, K. R. et al., Proteomic analysis of Acinetobacter Iwoffii K24 by 2-D gel electrophoresis and electrospray ionization quadrupole-time of flight mass spectrometry. J. Microbiol. Methods 2004, 57, 337-349.
45. Ramezani, M., MacIntosh, S. E., White, R. L., Utilization of D-amino acids by Fusobacterium nucleatum and Fusobacterium varium. Amino Acids 1999, 17, 185-193.
46. Gharbia, S. E., Shah, H. N., Welch, S. G., The influence of peptides on the uptake of amino acids in Fusobacterium; predicted interactions with Porphyromonas gingivalis. Curr. Microbiol. 1989, 19, 231-235.
47. Bearne, S. L., White, R. L., MacDonnell, J. E., Bahrami, S., Grønlund, J., Purification and characterization of β-methylaspartase from Fusobacterium varium. Mol. Cell. Biochem. 2001, 221, 117-126.
48. Foglesong, M. A., Cruden, D. L., Markovetz, A. J., Pleomorphism of fusobacteria isolated from the cockroach hindgut. J. Bacteriol. 1984, 158, 474-480.
49. Gharbia, S. E., Shah, H. N., Pathways of glutamate catabolism among Fusobacterium species. J. Gen. Microbiol. 1991, 137, 1201-1206.
50. Barker, H. A., Amino acid degradation by anaerobic bacteria. Annu. Rev. Biochem. 1981, 50, 23-40.
51. Barker, H. A., Kahn, J. M., Hedrick, L., Pathway of lysine degradation in Fusobacterium nucleatum. J. Bacteriol. 1982, 152, 201-207.
52. Choe, L. H., Lee, K. H., Quantitative and qualitative measure of intralaboratory two-dimensional protein gel reproducibility and the effects of sample preparation, sample load, and image analysis. Electrophoresis 2003, 24, 3500-3507.
53. Sambrook, J., Fritsch, E. F., Maniatis, T., Molecular Cloning, Cold Spring Harbor Laboratory Press, Plainview, New York 1989, pp. 1.21-21.52.
54. Gharbia, S. E., Shah, N., Glucose utilization and growth response to protein hydrolysates by Fusobacterium species. Curr. Microbiol. 1988, 17, 229-234.
55. McCarthy, J., Hopwood, F., Oxley, D., Laver, M. et al., Carbamylation of proteins in 2-D electrophoresis - myth or reality? J. Proteome Res. 2003, 2, 239-242.
56. Gharbia, S. E., Shah, H. N., Comparison of the amino acid uptake profile of reference and clinical isolates of Fusobacterium nucleatum subspecies. Oral Microbiol. Immunol. 1991, 6, 264-269.
57. Buckel, W., Unusual enzymes involved in five pathways of glutamate fermentation. Appl. Microbiol. Biotechnol. 2001, 57, 263-273.
58. White, R. L., Ramezani, M., Gharbia, S. E., Seth, R. et al., Stable-isotope studies of glutamate catabolism in Fusobacterium nucleatum. Biotechnol. Appl. Biochem. 1995, 22, 385-396.
59. Ahlman, B., Leijonmarck, C. E., Lind, C., Vinnars, E., Wernerman, J., Free amino acids in biopsy specimens from the human colonic mucosa. J. Surg. Res. 1993, 55, 647-653.
60. Stadtman, T. C., Lysine catabolism by clostridia. Adv. Enzymol. 1973, 38, 413-448.
61. Chang, C. H., Ballinger, M. D., Reed, G. H., Frey, P. A., Lysine 2,3-aminomutase: Rapid mix-freeze-quench electron paramagnetic resonance studies establishing the kinetic competence of a substrate-based radical intermediate. Biochemistry 1996, 35, 11081-11084.
62. 12 coenzyme dependent enzyme. Biochemistry 1973, 12, 1054-1063.
63. Chang, C. H., Frey, P. A., Cloning, sequencing, heterologous expression, purification, and characterization of adenosylcobalamin-dependent D-lysine 5, 6-aminomutase from Clostridium sticklandii. J. Biol. Chem. 2000, 275, 106-114.
64. Tang, K. H., Harms, A., Frey, P. A., Identification of a novel pyridoxal 5′-phosphate binding site in adenosylcobalamin-dependent lysine 5,6-aminomutase from Porphyromonas gingivalis. Biochemistry 2002, 41, 8767-8776.
65. Vasstrand, E. N., Hofstad, T., Endresen, C., Jensen, H. B., Demonstration of lanthionine as a natural constituent of the peptidoglycan of Fusobacterium nucleatum. Infect. Immun. 1979, 25, 775-780.
66. Fredriksen, A., Vasstrand, E. N., Jensen, H. B., Peptidoglycan precursor from Fusobacterium nucleatum contains lanthionine. J. Bacteriol. 1991, 73, 900-902.
67. Satyanarayana, S., Grossert, J. S., Lee, S. F., White, R. L., Determination of diamino acids in peptidoglycans from anaerobic bacteria. Amino Acids 2001, 21, 221-235.
68. Suzuki, H., Tamamura, R., Yajima, S., Kanno, M., Suguro, M., Corynebacterium sp. U-96 contains a cluster of genes of enzymes for the catabolism of sarcosine to pyruvate. Biosci. Biotechnol. Biochem. 2005, 69, 952-956.
69. Macfarlane, S., Macfarlane, G. T., Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 2003, 62, 67-72.
70. Diez-Gonzalez, F., Bond, D. R., Jennings, E., Russell, J. B., Alternative schemes of butyrate production in Butyrivibrio fibrisolvens and their relationship to acetate utilization, lactate production, and phylogeny. Arch. Microbiol. 1999, 171, 324-330.
71. Titgemeyer, F., Hillen, W., Global control of sugar metabolism: A gram-positive solution. Antonie Van Leeuwenhoek 2002, 82, 59-71.
72. 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. 1996, 178, 3015-3024.
73. Louis, P., Duncan, S. H., McCrae, S. I., Millar, J. et al., Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J. Bacteriol. 2004, 186, 2099-2106.
74. Asanuma, N., Ishiwata, M., Yoshii, T., Kikuchi, M. et al., Characterization and transcription of the genes involved in butyrate production in Butyrivibrio fibrisolvens type I and II strains. Curr. Microbiol. 2005, 51, 91-94.
75. Birch, R. M., O'Byrne, C., Booth, I. R., Cash, P., Enrichment of Escherichia coli proteins by column chromatography on reactive dye columns. Proteomics 2003, 3, 764-776.
76. von der Haar, T., McCarthy, J. E., Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function. Mol. Microbiol. 2002, 46, 531-544.
77. Takahashi, N., Sato, T., Dipeptide utilization by the periodontal pathogens Porphyromonas gingivalis, Prevotella intermedia, Prevotella nigrescens and Fusobacterium nucleatum. Oral Microbiol. Immunol. 2002, 17, 50-54.