1887

Abstract

This study characterized the two-component regulatory systems encoded by and , and assessed their influence on biofilm formation by 100-23. A method for deletion of multiple genes was employed to disrupt the genetic loci of two-component systems. The operons and showed complementary organization. Genes encode a histidine kinase, a response regulator and an ATP-binding cassette-type transporter with a bacteriocin-processing peptidase domain, respectively. Genes code for a signal peptide, a histidine kinase and a response regulator, respectively. Deletion of single or multiple genes in the operons and did not affect cell morphology, growth or the sensitivity to various stressors. However, gene disruption affected biofilm formation; this effect was dependent on the carbon source. Deletion of or increased sucrose-dependent biofilm formation . Glucose-dependent biofilm formation was particularly increased by deletion of . The expression of and was altered by deletion of , indicating cross-talk between these two regulatory systems. These results may contribute to our understanding of the genetic factors related to the biofilm formation and competitiveness of in intestinal ecosystems.

Funding
This study was supported by the:
  • , National Science and Engineering Council of Canada
  • , Canada Research Chairs
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2014-04-01
2021-03-08
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References

  1. Bairoch A., Apweiler R., Wu C. H., Barker W. C., Boeckmann B., Ferro S., Gasteiger E., Huang H., Lopez R. & other authors ( 2005). The Universal Protein Resource (UniProt). Nucleic Acids Res 33:D154–D159 [CrossRef][PubMed]
    [Google Scholar]
  2. Bijlsma J. J., Groisman E. A. ( 2003). Making informed decisions: regulatory interactions between two-component systems. Trends Microbiol 11:359–366 [CrossRef][PubMed]
    [Google Scholar]
  3. Boles B. R., Horswill A. R. ( 2008). Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052 [CrossRef][PubMed]
    [Google Scholar]
  4. Brunskill E. W., Bayles K. W. ( 1996). Identification and molecular characterization of a putative regulatory locus that affects autolysis in Staphylococcus aureus.. J Bacteriol 178:611–618[PubMed]
    [Google Scholar]
  5. Brurberg M. B., Nes I. F., Eijsink V. G. ( 1997). Pheromone-induced production of antimicrobial peptides in Lactobacillus.. Mol Microbiol 26:347–360 [CrossRef][PubMed]
    [Google Scholar]
  6. de Jong A., van Hijum S. A., Bijlsma J. J., Kok J., Kuipers O. P. ( 2006). BAGEL: a web-based bacteriocin genome mining tool. Nucleic Acids Res 34:Suppl 2W273–W279 [CrossRef][PubMed]
    [Google Scholar]
  7. Diep D. B., Håvarstein L. S., Nes I. F. ( 1996). Characterization of the locus responsible for the bacteriocin production in Lactobacillus plantarum C11. J Bacteriol 178:4472–4483[PubMed]
    [Google Scholar]
  8. Frese S. A., Benson A. K., Tannock G. W., Loach D. M., Kim J., Zhang M., Oh P. L., Heng N. C., Patil P. B. & other authors ( 2011). The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri.. PLoS Genet 7:e1001314 [CrossRef][PubMed]
    [Google Scholar]
  9. Frese S. A., Mackenzie D. A., Peterson D. A., Schmaltz R., Fangman T., Zhou Y., Zhang C., Benson A. K., Cody L. A. & other authors ( 2013). Molecular characterization of host-specific biofilm formation in a vertebrate gut symbiont. PLoS Genet 9:e1004057 [CrossRef][PubMed]
    [Google Scholar]
  10. Fujii T., Ingham C., Nakayama J., Beerthuyzen M., Kunuki R., Molenaar D., Sturme M., Vaughan E., Kleerebezem M., de Vos W. ( 2008). Two homologous Agr-like quorum-sensing systems cooperatively control adherence, cell morphology, and cell viability properties in Lactobacillus plantarum WCFS1. J Bacteriol 190:7655–7665 [CrossRef][PubMed]
    [Google Scholar]
  11. Fuller R. ( 1973). Ecological studies on the Lactobacillus flora associated with the crop epithelium of the fowl. J Appl Bacteriol 36:131–139 [CrossRef]
    [Google Scholar]
  12. Fuller R., Brooker B. E. ( 1974). Lactobacilli which attach to the crop epithelium of the fowl. Am J Clin Nutr 27:1305–1312[PubMed]
    [Google Scholar]
  13. Fuller R., Barrow P. A., Brooker B. E. ( 1978). Bacteria associated with the gastric epithelium of neonatal pigs. Appl Environ Microbiol 35:582–591[PubMed]
    [Google Scholar]
  14. Galperin M. Y. ( 2008). Telling bacteria: do not LytTR. Structure 16:657–659 [CrossRef][PubMed]
    [Google Scholar]
  15. Gänzle M. G., Höltzel A., Walter J., Jung G., Hammes W. P. ( 2000). Characterization of reutericyclin produced by Lactobacillus reuteri LTH2584. Appl Environ Microbiol 66:4325–4333 [CrossRef][PubMed]
    [Google Scholar]
  16. Hung J., Turner M. S., Walsh T., Giffard P. M. ( 2005). BspA (CyuC) in Lactobacillus fermentum BR11 is a highly expressed high-affinity L-cystine-binding protein. Curr Microbiol 50:33–37 [CrossRef][PubMed]
    [Google Scholar]
  17. Karatan E., Watnick P. ( 2009). Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347 [CrossRef][PubMed]
    [Google Scholar]
  18. Kuroda M., Ohta T., Uchiyama I., Baba T., Yuzawa H., Kobayashi I., Cui L., Oguchi A., Aoki K. & other authors ( 2001). Whole genome sequencing of meticillin-resistant Staphylococcus aureus.. Lancet 357:1225–1240 [CrossRef][PubMed]
    [Google Scholar]
  19. Loo C. Y., Corliss D. A., Ganeshkumar N. ( 2000). Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol 182:1374–1382 [CrossRef][PubMed]
    [Google Scholar]
  20. Mitrophanov A. Y., Groisman E. A. ( 2008). Signal integration in bacterial two-component regulatory systems. Genes Dev 22:2601–2611 [CrossRef][PubMed]
    [Google Scholar]
  21. Miyoshi Y., Okada S., Uchimura T., Satoh E. ( 2006). A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Biosci Biotechnol Biochem 70:1622–1628 [CrossRef][PubMed]
    [Google Scholar]
  22. Nikolskaya A. N., Galperin M. Y. ( 2002). A novel type of conserved DNA-binding domain in the transcriptional regulators of the AlgR/AgrA/LytR family. Nucleic Acids Res 30:2453–2459 [CrossRef][PubMed]
    [Google Scholar]
  23. Nobbs A. H., Lamont R. J., Jenkinson H. F. ( 2009). Streptococcus adherence and colonization. Microbiol Mol Biol Rev 73:407–450 [CrossRef][PubMed]
    [Google Scholar]
  24. Peng H. L., Novick R. P., Kreiswirth B., Kornblum J., Schlievert P. ( 1988). Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus.. J Bacteriol 170:4365–4372[PubMed]
    [Google Scholar]
  25. Perez-Casal J., Price J. A., Maguin E., Scott J. R. ( 1993). An M protein with a single C repeat prevents phagocytosis of Streptococcus pyogenes: use of a temperature-sensitive shuttle vector to deliver homologous sequences to the chromosome of S. pyogenes.. Mol Microbiol 8:809–819 [CrossRef][PubMed]
    [Google Scholar]
  26. Pfaffl M. W. ( 2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45 [CrossRef][PubMed]
    [Google Scholar]
  27. Quivey R. G., Kuhnert W. L., Hahn K. ( 2001). Genetics of acid adaptation in oral streptococci. Crit Rev Oral Biol Med 12:301–314 [CrossRef][PubMed]
    [Google Scholar]
  28. Roos S., Jonsson H. ( 2002). A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148:433–442[PubMed]
    [Google Scholar]
  29. Savage D. C., Dubos R., Schaedler R. W. ( 1968). The gastrointestinal epithelium and its autochthonous bacterial flora. J Exp Med 127:67–76 [CrossRef][PubMed]
    [Google Scholar]
  30. Schwab, C. (2006).Regulation and ecological relevance of fructosyltransferases inLactobacillus reuteri.
  31. Schwab C., Walter J., Tannock G. W., Vogel R. F., Gänzle M. G. ( 2007). Sucrose utilization and impact of sucrose on glycosyltransferase expression in Lactobacillus reuteri.. Syst Appl Microbiol 30:433–443 [CrossRef][PubMed]
    [Google Scholar]
  32. Senadheera D., Cvitkovitch D. G. ( 2008). Quorum sensing and biofilm formation by Streptococcus mutans.. Adv Exp Med Biol 631:178–188 [CrossRef][PubMed]
    [Google Scholar]
  33. Senadheera M. D., Lee A. W., Hung D. C., Spatafora G. A., Goodman S. D., Cvitkovitch D. G. ( 2007). The Streptococcus mutans vicX gene product modulates gtfB/C expression, biofilm formation, genetic competence, and oxidative stress tolerance. J Bacteriol 189:1451–1458 [CrossRef][PubMed]
    [Google Scholar]
  34. Sims I. M., Frese S. A., Walter J., Loach D., Wilson M., Appleyard K., Eason J., Livingston M., Baird M. & other authors ( 2011). Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100-23. ISME J 5:1115–1124 [CrossRef][PubMed]
    [Google Scholar]
  35. Siryaporn A., Goulian M. ( 2008). Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli.. Mol Microbiol 70:494–506 [CrossRef][PubMed]
    [Google Scholar]
  36. Su M. S., Schlicht S., Gänzle M. G. ( 2011). Contribution of glutamate decarboxylase in Lactobacillus reuteri to acid resistance and persistence in sourdough fermentation. Microb Cell Fact 10:Suppl 1S8 [CrossRef][PubMed]
    [Google Scholar]
  37. Su M. S., Oh P. L., Walter J., Gänzle M. G. ( 2012). Intestinal origin of sourdough Lactobacillus reuteri isolates as revealed by phylogenetic, genetic, and physiological analysis. Appl Environ Microbiol 78:6777–6780 [CrossRef][PubMed]
    [Google Scholar]
  38. Van Pijkeren J. P., Neoh K. M., Sirias D., Findley A. S., Britton R. A. ( 2012). Exploring optimization parameters to increase ssDNA recombineering in Lactococcus lactis and Lactobacillus reuteri.. Bioengineered 3:209–217 [CrossRef][PubMed]
    [Google Scholar]
  39. Vogel R. F., Knorr R., Müller M. R., Steudel U., Gänzle M. G., Ehrmann M. A. ( 1999). Non-dairy lactic fermentations: the cereal world. Antonie van Leeuwenhoek 76:403–411 [CrossRef][PubMed]
    [Google Scholar]
  40. Walter J. ( 2008). Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74:4985–4996 [CrossRef][PubMed]
    [Google Scholar]
  41. Walter J., Chagnaud P., Tannock G. W., Loach D. M., Dal Bello F., Jenkinson H. F., Hammes W. P., Hertel C. ( 2005). A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl Environ Microbiol 71:979–986 [CrossRef][PubMed]
    [Google Scholar]
  42. Walter J., Loach D. M., Alqumber M., Rockel C., Hermann C., Pfitzenmaier M., Tannock G. W. ( 2007). d-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract. Environ Microbiol 9:1750–1760 [CrossRef][PubMed]
    [Google Scholar]
  43. Walter J., Schwab C., Loach D. M., Gänzle M. G., Tannock G. W. ( 2008). Glucosyltransferase A (GtfA) and inulosucrase (Inu) of Lactobacillus reuteri TMW1.106 contribute to cell aggregation, in vitro biofilm formation, and colonization of the mouse gastrointestinal tract. Microbiology 154:72–80 [CrossRef][PubMed]
    [Google Scholar]
  44. Walter J., Britton R. A., Roos S. ( 2011). Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A 108:Suppl 14645–4652 [CrossRef][PubMed]
    [Google Scholar]
  45. Ween O., Teigen S., Gaustad P., Kilian M., Håvarstein L. S. ( 2002). Competence without a competence pheromone in a natural isolate of Streptococcus infantis.. J Bacteriol 184:3426–3432 [CrossRef][PubMed]
    [Google Scholar]
  46. Wesney E., Tannock G. W. ( 1979). Association of rat, pig, and fowl biotypes of lactobacilli with the stomach of gnotobiotic mice. Microb Ecol 5:35–42 [CrossRef][PubMed]
    [Google Scholar]
  47. Wilson C. M., Aggio R. B. M., O’Toole P. W., Villas-Boas S., Tannock G. W. ( 2012). Transcriptional and metabolomic consequences of luxS inactivation reveal a metabolic rather than quorum-sensing role for LuxS in Lactobacillus reuteri 100-23. J Bacteriol 194:1743–1746 [CrossRef][PubMed]
    [Google Scholar]
  48. Yuki N., Shimazaki T., Kushiro A., Watanabe K., Uchida K., Yuyama T., Morotomi M. ( 2000). Colonization of the stratified squamous epithelium of the nonsecreting area of horse stomach by lactobacilli. Appl Environ Microbiol 66:5030–5034 [CrossRef][PubMed]
    [Google Scholar]
  49. Zhang Z. G., Ye Z. Q., Yu L., Shi P. ( 2011). Phylogenomic reconstruction of lactic acid bacteria: an update. BMC Evol Biol 11:1–12 [CrossRef][PubMed]
    [Google Scholar]
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