1887

Abstract

Host–bacteria interactions are often mediated via surface-associated proteins. The identification of these proteins is an important goal of bacterial proteomics. To address how bile can influence the cell-envelope proteome of biotype NCIMB 8809, we analysed its membrane protein fraction using stable isotope labelling of amino acids in cell culture (SILAC). We were able to identify 141 proteins in the membrane fraction, including a large percentage of the theoretical transporters of this species. Moreover, the envelope-associated soluble fraction was analysed using different subfractionation techniques and differential in-gel fluorescence electrophoresis (DIGE). This approach identified 128 different proteins. Some of them were well-known cell wall proteins, but others were highly conserved cytoplasmic proteins probably displaying a ‘moonlighting’ function. We were able to identify 11 proteins in the membrane fraction and 6 proteins in the envelope-associated soluble fraction whose concentration varied in the presence of bile. Bile promoted changes in the levels of proteins with important biological functions, such as some ribosomal proteins and enolase. Also, oligopeptide-binding proteins were accumulated on the cell surface, which was reflected in a different tripeptide transport rate in the cells grown with bile. The data reported here will provide the first cell-envelope proteome map for , and may contribute to understanding the bile tolerance of these bacteria.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.024273-0
2009-03-01
2020-01-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/3/957.html?itemId=/content/journal/micro/10.1099/mic.0.024273-0&mimeType=html&fmt=ahah

References

  1. Antikainen, J., Kuparinen, V., Lähteenmäki, K. & Korhonen, T. K. ( 2007; ). pH-dependent association of enolase and glyceraldehyde-3-phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids. J Bacteriol 189, 4539–4543.[CrossRef]
    [Google Scholar]
  2. Bateman, A., Coin, L., Durbin, R., Finn, R. D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S. & other authors ( 2004; ). The Pfam protein families database. Nucleic Acids Res 32, D138–D141.[CrossRef]
    [Google Scholar]
  3. Begley, M., Gahan, C. G. & Hill, C. ( 2005; ). The interaction between bacteria and bile. FEMS Microbiol Rev 29, 625–651.[CrossRef]
    [Google Scholar]
  4. Buist, G., Ridder, A. N., Kok, J. & Kuipers, O. P. ( 2006; ). Different subcellular locations of secretome components of Gram-positive bacteria. Microbiology 152, 2867–2874.[CrossRef]
    [Google Scholar]
  5. Bunai, K. & Yamane, K. ( 2005; ). Effectiveness and limitation of two-dimensional gel electrophoresis in bacterial membrane protein proteomics and perspectives. J Chromatogr B Analyt Technol Biomed Life Sci 815, 227–236.[CrossRef]
    [Google Scholar]
  6. Candela, M., Bergmann, S., Vici, M., Vitali, B., Turroni, S., Eikmanns, B. J., Hammerschmidt, S. & Brigidi, P. ( 2007; ). Binding of human plasminogen to Bifidobacterium. J Bacteriol 189, 5929–5936.[CrossRef]
    [Google Scholar]
  7. Chen, H., Teplitski, M., Robinson, J. B., Rolfe, B. G. & Bauer, W. D. ( 2003; ). Proteomic analysis of wild-type Sinorhizobium meliloti responses to N-acyl homoserine lactone quorum-sensing signals and the transition to stationary phase. J Bacteriol 185, 5029–5036.[CrossRef]
    [Google Scholar]
  8. Couté, Y., Hernandez, C., Appel, R. D., Sanchez, J. C. & Margolles, A. ( 2007; ). Labeling of Bifidobacterium longum cells with 13C-substituted leucine for quantitative proteomic analyses. Appl Environ Microbiol 73, 5653–5656.[CrossRef]
    [Google Scholar]
  9. Detmers, F. J., Kunji, E. R., Lanfermeijer, F. C., Poolman, B. & Konings, W. N. ( 1998; ). Kinetics and specificity of peptide uptake by the oligopeptide transport system of Lactococcus lactis. Biochemistry 37, 16671–16679.[CrossRef]
    [Google Scholar]
  10. Dreisbach, A., Otto, A., Becher, D., Hammer, E., Teumer, A., Gouw, J. W., Hecker, M. & Völker, U. ( 2008; ). Monitoring of changes in the membrane proteome during stationary phase adaptation of Bacillus subtilis using in vivo labeling techniques. Proteomics 8, 2062–2076.[CrossRef]
    [Google Scholar]
  11. Eymann, C., Dreisbach, A., Albrecht, D., Bernhardt, J., Becher, D., Gentner, S., Tam le, T., Büttner, K., Buurman, G. & other authors ( 2004; ). A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 4, 2849–2876.[CrossRef]
    [Google Scholar]
  12. Fujiwara, S., Hashiba, H., Hirota, T. & Forstner, J. F. ( 1997; ). Proteinaceous factor(s) in culture supernatant fluids of bifidobacteria which prevents the binding of enterotoxigenic Escherichia coli to gangliotetraosylceramide. Appl Environ Microbiol 63, 506–512.
    [Google Scholar]
  13. Granato, D., Bergonzelli, G. E., Pridmore, R. D., Marvin, L., Rouvet, M. & Corthésy-Theulaz, I. E. ( 2004; ). Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun 72, 2160–2169.[CrossRef]
    [Google Scholar]
  14. Gueimonde, M., Tölkkö, S., Korpimäki, T. & Salminen, S. ( 2004; ). New real-time quantitative PCR procedure for quantification of bifidobacteria in human fecal samples. Appl Environ Microbiol 70, 4165–4169.[CrossRef]
    [Google Scholar]
  15. Gueimonde, M., Noriega, L., Margolles, A., de los Reyes-Gavilán, C. G. & Salminen, S. ( 2005; ). Ability of Bifidobacterium strains with acquired resistance to bile to adhere to human intestinal mucus. Int J Food Microbiol 101, 341–346.[CrossRef]
    [Google Scholar]
  16. Harmsen, H. J., Wildeboer-Veloo, A. C., Raangs, G. C., Wagendorp, A. A., Klijn, N., Bindels, J. G. & Welling, G. W. ( 2000; ). Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30, 61–67.[CrossRef]
    [Google Scholar]
  17. Hoarau, C., Lagaraine, C., Martin, L., Velge-Roussel, F. & Lebranchu, Y. ( 2006; ). Supernatant of Bifidobacterium breve induces dendritic cell maturation, activation, and survival through a Toll-like receptor 2 pathway. J Allergy Clin Immunol 117, 696–702.[CrossRef]
    [Google Scholar]
  18. Hoarau, C., Martin, L., Faugaret, D., Baron, C., Dauba, A., Aubert-Jacquin, C., Velge-Roussel, F. & Lebranchu, Y. ( 2008; ). Supernatant from Bifidobacterium differentially modulates transduction signaling pathways for biological functions of human dendritic cells. PLoS One 3, e2753 [CrossRef]
    [Google Scholar]
  19. Hofmann, A. F. ( 1999; ). The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med 159, 2647–2658.[CrossRef]
    [Google Scholar]
  20. Ivanov, D., Emonet, C., Foata, F., Affolter, M., Delley, M., Fisseha, M., Blum-Sperisen, S., Kochhar, S. & Arigoni, F. ( 2006; ). A serpin from the gut bacterium Bifidobacterium longum inhibits eukaryotic elastase-like serine proteases. J Biol Chem 281, 17246–17252.[CrossRef]
    [Google Scholar]
  21. Jamieson, D. J. & Higgins, C. F. ( 1984; ). Anaerobic and leucine-dependent expression of a peptide transport gene in Salmonella typhimurium. J Bacteriol 160, 131–136.
    [Google Scholar]
  22. Jang, J. H. & Hanash, S. ( 2003; ). Profiling of the cell surface proteome. Proteomics 3, 1947–1954.[CrossRef]
    [Google Scholar]
  23. Jeffery, C. J. ( 2003; ). Moonlighting proteins: old proteins learning new tricks. Trends Genet 19, 415–417.[CrossRef]
    [Google Scholar]
  24. Kelly, D., Conway, S. & Aminov, R. ( 2005a; ). Commensal gut bacteria: mechanisms of immune modulation. Trends Immunol 26, 326–333.[CrossRef]
    [Google Scholar]
  25. Kelly, P., Maguire, P. B., Bennett, M., Fitzgerald, D. J., Edwards, R. J., Thiede, B., Treumann, A., Collins, J. K., O'Sullivan, G. C. & other authors ( 2005b; ). Correlation of probiotic Lactobacillus salivarius growth phase with its cell wall-associated proteome. FEMS Microbiol Lett 252, 153–159.[CrossRef]
    [Google Scholar]
  26. Knaust, A., Weber, M. V., Hammerschmidt, S., Bergmann, S., Frosch, M. & Kurzai, O. ( 2007; ). Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitidis. J Bacteriol 189, 3246–3255.[CrossRef]
    [Google Scholar]
  27. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. ( 2001; ). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305, 567–580.[CrossRef]
    [Google Scholar]
  28. Langendijk, P. S., Schut, F., Jansen, G. J., Raangs, G. C., Kamphuis, G. R., Wilkinson, M. H. & Welling, G. W. ( 1995; ). Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61, 3069–3075.
    [Google Scholar]
  29. Madera, M., Vogel, C., Kummerfeld, S. K., Chothia, C. & Gough, J. ( 2004; ). The SUPERFAMILY database in 2004: additions and improvements. Nucleic Acids Res 32, D235–D239.[CrossRef]
    [Google Scholar]
  30. Marco, M. L., Pavan, S. & Kleerebezem, M. ( 2006; ). Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 17, 204–210.[CrossRef]
    [Google Scholar]
  31. Marouga, R., David, S. & Hawkins, E. ( 2005; ). The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem 382, 669–678.[CrossRef]
    [Google Scholar]
  32. Masco, L., Huys, G., De Brandt, E., Temmerman, R. & Swings, J. ( 2005; ). Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. Int J Food Microbiol 102, 221–230.[CrossRef]
    [Google Scholar]
  33. Mitsuma, T., Odajima, H., Momiyama, Z., Watanabe, K., Masuguchi, M., Sekine, T., Shidara, S. & Hirano, S. ( 2008; ). Enhancement of gene expression by a peptide p(CHWPR) produced by Bifidobacterium lactis BB-12. Microbiol Immunol 52, 144–155.[CrossRef]
    [Google Scholar]
  34. Molloy, M. P., Herbert, B. R., Slade, M. B., Rabilloud, T., Nouwens, A. S., Williams, K. L. & Gooley, A. A. ( 2000; ). Proteomic analysis of the Escherichia coli outer membrane. Eur J Biochem 267, 2871–2881.[CrossRef]
    [Google Scholar]
  35. Mukai, T., Kaneko, S., Matsumoto, M. & Ohori, H. ( 2004; ). Binding of Bifidobacterium bifidum and Lactobacillus reuteri to the carbohydrate moieties of intestinal glycolipids recognized by peanut agglutinin. Int J Food Microbiol 90, 357–362.[CrossRef]
    [Google Scholar]
  36. Nandakumar, R., Nandakumar, M. P., Marten, M. R. & Ross, J. M. ( 2005; ). Proteome analysis of membrane and cell wall associated proteins from Staphylococcus aureus. J Proteome Res 4, 250–257.[CrossRef]
    [Google Scholar]
  37. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A. & Mann, M. ( 2002; ). Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1, 376–386.[CrossRef]
    [Google Scholar]
  38. O'Riordan, K. & Fitzgerald, G. F. ( 1998; ). Evaluation of bifidobacteria for the production of antimicrobial compounds and assessment of performance in cottage cheese at refrigeration temperature. J Appl Microbiol 85, 103–114.[CrossRef]
    [Google Scholar]
  39. Rivera-Amill, V., Kim, B. J., Seshu, J. & Konkel, M. E. ( 2001; ). Secretion of the virulence-associated Campylobacter invasion antigens from Campylobacter jejuni requires a stimulatory signal. J Infect Dis 183, 1607–1616.[CrossRef]
    [Google Scholar]
  40. Rodríguez-Ortega, M. J., Norais, N., Bensi, G., Liberatori, S., Capo, S., Mora, M., Scarselli, M., Doro, F., Ferrari, G. & other authors ( 2006; ). Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat Biotechnol 24, 191–197.[CrossRef]
    [Google Scholar]
  41. Ruiz, L., Sánchez, B., Ruas-Madiedo, P., de los Reyes-Gavilán, C. G. & Margolles, A. ( 2007; ). Cell envelope changes in Bifidobacterium animalis ssp. lactis as a response to bile. FEMS Microbiol Lett 274, 316–322.[CrossRef]
    [Google Scholar]
  42. Salminen, S. J., Gueimonde, M. & Isolauri, E. ( 2005; ). Probiotics that modify disease risk. J Nutr 135, 1294–1298.
    [Google Scholar]
  43. Sánchez, B., Noriega, L., Ruas-Madiedo, P., de los Reyes-Gavilán, C. G. & Margolles, A. ( 2004; ). Acquired resistance to bile increases fructose-6-phosphate phosphoketolase activity in Bifidobacterium. FEMS Microbiol Lett 235, 35–41.[CrossRef]
    [Google Scholar]
  44. Sánchez, B., Champomier-Vergès, M. C., Anglade, P., Baraige, F., de los Reyes-Gavilán, C. G., Margolles, A. & Zagorec, M. ( 2005; ). Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J Bacteriol 187, 5799–5808.[CrossRef]
    [Google Scholar]
  45. Sánchez, B., de los Reyes-Gavilán, C. G. & Margolles, A. ( 2006; ). The F1F0-ATPase of Bifidobacterium animalis is involved in bile tolerance. Environ Microbiol 8, 1825–1833.[CrossRef]
    [Google Scholar]
  46. Sánchez, B., Champomier-Vergès, M. C., Collado, M. C., Anglade, P., Baraige, F., Sanz, Y., de los Reyes-Gavilán, C. G., Margolles, A. & Zagorec, M. ( 2007; ). Low-pH adaptation and the acid tolerance response of Bifidobacterium longum biotype longum. Appl Environ Microbiol 73, 6450–6459.[CrossRef]
    [Google Scholar]
  47. Sánchez, B., Champomier-Vergès, M. C., Anglade, P., Baraige, F., de los Reyes-Gavilán, C. G., Margolles, A. & Zagorec, M. ( 2008; ). A preliminary analysis of Bifidobacterium longum exported proteins by two-dimensional electrophoresis. J Mol Microbiol Biotechnol 14, 74–79.[CrossRef]
    [Google Scholar]
  48. Schaumburg, J., Diekmann, O., Hagendorff, P., Bergmann, S., Rohde, M., Hammerschmidt, S., Jänsch, L., Wehland, J. & Kärst, U. ( 2004; ). The cell wall subproteome of Listeria monocytogenes. Proteomics 4, 2991–3006.[CrossRef]
    [Google Scholar]
  49. Schell, M. A., Karmirantzou, M., Snel, B., Vilanova, D., Berger, B., Pessi, G., Zwahlen, M. C., Desiere, F., Bork, P. & other authors ( 2002; ). The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A 99, 14422–14427.[CrossRef]
    [Google Scholar]
  50. Severin, A., Nickbarg, E., Wooters, J., Quazi, S. A., Matsuka, Y. V., Murphy, E., Moutsatsos, I. K., Zagursky, R. J. & Olmsted, S. B. ( 2007; ). Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J Bacteriol 189, 1514–1522.[CrossRef]
    [Google Scholar]
  51. Silveira, M. G., Baumgärtner, M., Rombouts, F. M. & Abee, T. ( 2004; ). Effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni. Appl Environ Microbiol 70, 2748–2755.[CrossRef]
    [Google Scholar]
  52. Speers, A. E. & Wu, C. C. ( 2007; ). Proteomics of integral membrane proteins – theory and application. Chem Rev 107, 3687–3714.[CrossRef]
    [Google Scholar]
  53. Spence, J. M. & Clark, V. L. ( 2000; ). Role of ribosomal protein L12 in gonococcal invasion of Hec1B cells. Infect Immun 68, 5002–5010.[CrossRef]
    [Google Scholar]
  54. Sutcliffe, I. C. & Harrington, D. J. ( 2002; ). Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes. Microbiology 148, 2065–2077.
    [Google Scholar]
  55. Tjalsma, H., Lambooy, L., Hermans, P. W. & Swinkels, D. W. ( 2008; ). Shedding & shaving: disclosure of proteomic expressions on a bacterial face. Proteomics 8, 1415–1428.[CrossRef]
    [Google Scholar]
  56. VanBogelen, R. A. & Neidhardt, F. C. ( 1990; ). Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A 87, 5589–5593.[CrossRef]
    [Google Scholar]
  57. Wilson, D. N. & Nierhaus, K. H. ( 2005; ). Ribosomal proteins in the spotlight. Crit Rev Biochem Mol Biol 40, 243–267.[CrossRef]
    [Google Scholar]
  58. Wolff, S., Antelmann, H., Albrecht, D., Becher, D., Bernhardt, J., Bron, S., Büttner, K., van Dijl, J. M., Eymann, C. & other authors ( 2007; ). Towards the entire proteome of the model bacterium Bacillus subtilis by gel-based and gel-free approaches. J Chromatogr B Analyt Technol Biomed Life Sci 849, 129–140.[CrossRef]
    [Google Scholar]
  59. Wouters, J. A., Hain, T., Darji, A., Hüfner, E., Wemekamp-Kamphuis, H., Chakraborty, T. & Abee, T. ( 2005; ). Identification and characterization of di- and tripeptide transporter DtpT of Listeria monocytogenes EGD-e. Appl Environ Microbiol 71, 5771–5778.[CrossRef]
    [Google Scholar]
  60. Yuan, J., Wang, B., Sun, Z., Bo, X., Yuan, X., He, X., Zhao, H., Du, X., Wang, F. & other authors ( 2008; ). Analysis of host-inducing proteome changes in Bifidobacterium longum NCC2705 grown in vivo. J Proteome Res 7, 3753–3785.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.024273-0
Loading
/content/journal/micro/10.1099/mic.0.024273-0
Loading

Data & Media loading...

Supplements

Predicted location of the proteins identified in the membrane fraction of the cell envelope [ Excel file] (93 kb) Predicted location of the proteins identified in the soluble fraction of the cell envelope [ Excel file] (75 kb) Quantitative analysis of proteins from the enzymatic and SDS fractions [ PDF] (26 kb)

EXCEL

Predicted location of the proteins identified in the membrane fraction of the cell envelope [ Excel file] (93 kb) Predicted location of the proteins identified in the soluble fraction of the cell envelope [ Excel file] (75 kb) Quantitative analysis of proteins from the enzymatic and SDS fractions [ PDF] (26 kb)

EXCEL

Predicted location of the proteins identified in the membrane fraction of the cell envelope [ Excel file] (93 kb) Predicted location of the proteins identified in the soluble fraction of the cell envelope [ Excel file] (75 kb) Quantitative analysis of proteins from the enzymatic and SDS fractions [ PDF] (26 kb)

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error