Effect of alkaline growth pH on the expression of cell envelope proteins in Fusobacterium nucleatum

Microbiology

Volumn 156, Issue 6, 2010, Pages 1783-1794

  Zilm, Peter S ^a   Mira, Alex ^b   Bagley, Christopher J ^a,c   Rogers, Anthony H ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b Centre for Public Health Research CSISP   (Spain)

^c Hospira Adelaide   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACID DERIVATIVE; CHAPERONE; CYTOPLASM PROTEIN; GLUTAMIC ACID; IRON; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; PHOSPHATE; PORIN; VIRULENCE FACTOR;

ADAPTATION; ALKALINITY; AMINO ACID METABOLISM; ARTICLE; BACTERIAL GROWTH; CATABOLISM; CHEMOSTAT; CONTROLLED STUDY; DOWN REGULATION; ENERGY YIELD; FUSOBACTERIUM NUCLEATUM; GRAM NEGATIVE BACTERIUM; HORIZONTAL GENE TRANSFER; IRON TRANSPORT; MOUTH FLORA; NONHUMAN; PERIODONTAL DISEASE; PERIODONTITIS; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

BACTERIAL OUTER MEMBRANE PROTEINS; FUSOBACTERIUM NUCLEATUM; GENE EXPRESSION REGULATION, BACTERIAL; GINGIVA; HYDROGEN-ION CONCENTRATION; PERIPLASM; PROTEOME; VIRULENCE;

EID: 77953184633     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.035881-0     Document Type: Article

References (55)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
2. Barker, H. A. (1981). Amino acid degradation by anaerobic bacteria. Annu Rev Biochem 50, 23-40.
3. Bartold, P. M., Gully, N. J., Zilm, P. S. & Rogers, A. H. (1991). Identification of components in Fusobacterium nucleatum chemostatculture supernatants that are potent inhibitors of human gingival fibroblast proliferation. J Periodontal Res 26, 314-322.
4. Berven, F. S., Flikka, K., Jensen, H. B. & Eidhammer, I. (2004). BOMP: a program to predict integral beta-barrel outer membrane proteins encoded within genomes of Gram-negative bacteria. Nucleic Acids Res 32, W394-W399.
5. Bickel, M. & Cimasoni, G. (1985). The pH of human crevicular fluid measured by a new microanalytical technique. J Periodontal Res 20, 35-40.
6. Campostrini, N., Areces, L. B., Rappsilber, J., Pietrogrande, M. C., Dondi, F., Pastorino, F., Ponzoni, M. & Righetti, P. G. (2005). Spot overlapping in two-dimensional maps: a serious problem ignored for much too long. Proteomics 5, 2385-2395.
7. Conrads, G. (2002). DNA probes and primers in dental practice. Clin Infect Dis 35, S72-S77.
8. Cordwell, S. J. (2006). Technologies for bacterial surface proteomics. Curr Opin Microbiol 9, 320-329.
9. Diaz, P. I., Zilm, P. S. & Rogers, A. H. (2002). Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbon dioxide-depleted environments. Microbiology 148, 467-472.
10. Dzink, J. L., Sheenan, M. T. & Socransky, S. S. (1990). Proposal of three subspecies of Fusobacterium nucleatum Knorr 1922: Fusobacterium nucleatum subsp. nucleatum subsp. nov., comb. nov.; Fusobacterium nucleatum subsp. polymorphum subsp. nov., nom. rev., comb. nov.; and Fusobacterium nucleatum subsp. vincentii subsp. nov., nom. rev., comb. nov. Int J Syst Bacteriol 40, 74-78.
11. Eggert, F. M., Drewell, L., Bigelow, J. A., Speck, J. E. & Goldner, M. (1991). The pH of gingival crevices and periodontal pockets in children, teenagers and adults. Arch Oral Biol 36, 233-238.
12. Ellwood, D. C. & Hunter, J. R. (1976). The mouth as a chemostat. In Continuous Culture 6: Applications and New Fields, pp. 270-282. Edited by A. C. R. Dean, D. C. Ellwood, C. G. T. Ebvans & J. Melling. Chichester, UK: Ellis Horwood.
13. Forward, J. A., Behrendt, M. C., Wyborn, N. R., Cross, R. & Kelly, D. J. (1997). TRAP transporters: a new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobacter capsulatus and by homologs in diverse Gram-negative bacteria. J Bacteriol 179, 5482-5493. (Pubitemid 27387619)
14. Garcia-Vallve, S., Romeu, A. & Palau, J. (2000). Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res 10, 1719-1725.
15. Gardy, J. L., Laird, M. R., Chen, F., Rey, S., Walsh, C. J., Ester, M. & Brinkman, F. S. (2005). PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21, 617-623.
16. Gharbia, S. E. & Shah, H. N. (1992). Fusobacterium nucleatum subsp. fusiforme subsp. nov. and Fusobacterium nucleatum subsp. animalis subsp. nov. as additional subspecies within Fusobacterium nucleatum. Int J Syst Bacteriol 42, 296-298.
17. Gmur, R., Munson, M. A. & Wade, W. G. (2006). Genotypic and phenotypic characterization of fusobacteria from Chinese and European patients with inflammatory periodontal diseases. Syst Appl Microbiol 29, 120-130.
18. Goldstein, E. J., Summanen, P. H., Citron, D. M., Rosove, M. H. & Finegold, S. M. (1995). Fatal sepsis due to a beta-lactamase-producing strain of Fusobacterium nucleatum subspecies polymorphum. Clin Infect Dis 20, 797-800.
19. Hamilton, I. R., Phipps, P. J. & Ellwood, D. C. (1979). Effect of growth rate and glucose concentration on the biochemical properties of Streptococcus mutans Ingbritt in continuous culture. Infect Immun 26, 861-869.
20. Hoskisson, P. A. & Hobbs, G. (2005). Continuous culture - making a comeback? Microbiology 151, 3153-3159.
21. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J. & Mann, M. (2005). Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4, 1265-1272.
22. Kapatral, V., Anderson, I., Ivanova, N., Reznik, G., Los, T., Lykidis, A., Bhattacharyya, A., Bartman, A., Gardner, W. & other authors (2002). Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 184, 2005-2018.
23. Kapatral, V., Ivanova, N., Anderson, I., Reznik, G., Bhattacharyya, A., Gardner, W. L., Mikhailova, N., Lapidus, A., Larsen, N. & other authors (2003). Genome analysis of F. nucleatum sub spp vincentii and its comparison with the genome of F. nucleatum ATCC 25586. Genome Res 13, 1180-1189.
24. Karpathy, S. E., Qin, X., Gioia, J., Jiang, H., Liu, Y., Petrosino, J. F., Yerrapragada, S., Fox, G. E., Haake, S. K. & other authors (2007). Genome sequence of Fusobacterium nucleatum subspecies polymorphum - a genetically tractable fusobacterium. PLoS One 2, e659.
25. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
26. Legault, B. A., Lopez-Lopez, A., Alba-Casado, J. C., Doolittle, W. F., Bolhuis, H., Rodriguez-Valera, F. & Papke, R. T. (2006). Environmental genomics of "Haloquadratum walsbyi" in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species. BMC Genomics 7, 171.
27. Marsh, P. D., McKee, A. S. & McDermid, A. S. (1993). Continuous culture studies. In Biology of the Species Porphyromonas gingivalis. Edited by N. H. Shah, D. Mayrand & R. J. Genco. Boca Raton, FL: CRC Press.
28. Marsh, P. D., McDermid, A. S., McKee, A. S. & Baskerville, A. (1994). The effect of growth rate and haemin on the virulence and proteolytic activity of Porphyromonas gingivalis W50. Microbiology 140, 861-865.
29. Matsuzaki, M., Kiso, Y., Yamamoto, I. & Satoh, T. (2000). Gene disruption analysis of DppA isolated as a periplasmic molecular chaperone-like protein for folding of dimethyl sulfoxide reductase in Rhodobacter sphaeroides f. sp. denitrificans. FEMS Microbiol Lett 193, 223-229.
30. McDermid, A. S., McKee, A. S. & Marsh, P. D. (1988). Effect of environmental pH on enzyme activity and growth of Bacteroides gingivalis W50. Infect Immun 56, 1096-1100.
31. McKee, A. S., McDermid, A. S., Baskerville, A., Dowsett, A. B., Ellwood, D. C. & Marsh, P. D. (1986). Effect of hemin on the physiology and virulence of Bacteroides gingivalis W50. Infect Immun 52, 349-355. (Pubitemid 16117785)
32. Mira, A. (2008). Horizontal gene transfer in oral bacteria. In Molecular Oral Microbiology, chapter 3, pp. 65-85. Edited by A. H. Rogers. Norwich, UK: Horizon Scientific Press.
33. Mira, A., Pushker, R., Legault, B. A., Moreira, D. & Rodriguez-Valera, F. (2004). Evolutionary relationships of Fusobacterium nucleatum based on phylogenetic analysis and comparative genomics. BMC Evol Biol 4, 50.
34. Morris, M. L., Andrews, R. H. & Rogers, A. H. (1996). The use of allozyme electrophoresis to assess genetic heterogeneity among previously subspeciated isolates of Fusobacterium nucleatum. Oral Microbiol Immunol 11, 15-21. (Pubitemid 3026851)
35. Pushker, R., Mira, A. & Rodríguez-Valera, F. (2004). Comparative genomics of gene-family size in closely related bacteria. Genome Biol 5, R27.
36. Rogers, A. H., Zilm, P. S. & Gully, N. J. (1986). The utilisation of arginine by oral streptococci grown glucose-limited in a chemostat. FEMS Microbiol Lett 37, 9-13.
37. Rogers, A. H., Zilm, P. S., Gully, N. J., Pfennig, A. L. & Marsh, P. D. (1991). Aspects of the growth and metabolism of Fusobacterium nucleatum ATCC 10953 in continuous culture. Oral Microbiol Immunol 6, 250-255.
38. Rogers, A. H., Gully, N. J., Pfennig, A. L. & Zilm, P. S. (1992). The breakdown and utilization of peptides by strains of Fusobacterium nucleatum. Oral Microbiol Immunol 7, 299-303.
39. Rowley, G., Spector, M., Kormanec, J. & Roberts, M. (2006). Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat Rev Microbiol 4, 383-394.
40. Ruby, J. & Goldner, M. (2007). Nature of symbiosis in oral disease. J Dent Res 86, 8-11.
41. Sanchez-Perez, G., Mira, A., Nyiro, G., Pasic, L. & Rodriguez-Valera, F. (2008). Adapting to environmental changes using specialized paralogs. Trends Genet 24, 154-158.
42. Santoyo, G. & Romero, D. (2005). Gene conversion and concerted evolution in bacterial genomes. FEMS Microbiol Rev 29, 169-183.
43. Socransky, S. S. & Haffajee, A. D. (2005). Periodontal microbial ecology. Periodontol 2000 38, 135-187.
44. Socransky, S. S., Manganiello, A. D., Propas, D., Oram, V. & van Houte, J. (1977). Bacteriological studies of developing supragingival dental plaque. J Periodontal Res 12, 90-106.
45. Socransky, S. S., Haffajee, A. D., Cugini, M. A., Smith, C. & Kent, R. L., Jr (1998). Microbial complexes in subgingival plaque. J Clin Periodontol 25, 134-144.
46. Sorek, R., Zhu, Y., Creevey, C. J., Francino, M. P., Bork, P. & Rubin, E.M. (2007). Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318, 1449-1452.
47. Takahashi, N. (2003). Acid-neutralizing activity during amino acid fermentation by Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum. Oral Microbiol Immunol 18, 109-113.
48. Takahashi, N. (2005). Microbial ecosystem in the oral cavity: metabolic diversity in an ecological niche and its relationship with oral diseases. Int Congr Ser 1284, 103-112.
49. Tempest, D. W. (1969). The continuous culture of micro-organisms. I. Theory of the chemostat. In Methods in Microbiology, vol. 2, pp. 260-276. Edited by J. R. Norris & D. W. Ribbons. Salisbury, UK: Microbiology Research Establishment.
50. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
51. van der Hoeven, J. S., de Jong, M. H., Camp, P. J. M. & van den Kieboom, C. W. A. (1985). Competition between oral Streptococcus species in the chemostat under alternating conditions of glucose limitation and excess. FEMS Microbiol Ecol 31, 373-379.
52. Vroom, J. M., De Grauw, K. J., Gerritsen, H. C., Bradshaw, D. J., Marsh, P. D., Watson, G. K., Birmingham, J. J. & Allison, C. (1999). Depth penetration and detection of pH gradients in biofilms by twophoton excitation microscopy. Appl Environ Microbiol 65, 3502-3511.
53. Zhang, Y., Wang, T., Chen, W., Yilmaz, O., Park, Y., Jung, I. Y., Hackett, M. & Lamont, R. J. (2005). Differential protein expression by Porphyromonas gingivalis in response to secreted epithelial cell components. Proteomics 5, 198-211.
54. Zilm, P. S. & Rogers, A. H. (2007). Co-adhesion and biofilm formation by Fusobacterium nucleatum in response to growth pH. Anaerobe 13, 146-152.
55. Zilm, P. S., Bagley, C. J., Rogers, A. H., Milne, I. R. & Gully, N. J. (2007). The proteomic profile of Fusobacterium nucleatum is regulated by growth pH. Microbiology 153, 148-159.