Connection between Hexuronate Metabolism and the Ability of Escherichia coli to Adhesion and Biofilm Formation

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The formation of bacterial biofilms is an important factor of the chronic infection development, which requires the search for effective ways to prevent it. Here, it was found that hexuronates did not affect the biofilm formation by the probiotic strain Escherichia coli Nissle 1917 and its adhesive properties but reduced the efficiency of biofilm formation by the E. coli K-12 MG1655 strain, enhancing its adhesion to human intestinal carcinoma cells. It was shown that the regulators of hexuronate metabolism, UxuR and YjjM, are involved, along with cAMP-CRP, in the control of motility, adhesion and biofilm formation of E. coli K-12 MG1655. In addition, untranslated RNAs encoded in the uxuR gene play an important role inhibiting the main sigma factor of motility.

Full Text

Restricted Access

About the authors

T. A. Bessonova

Institute of Cell Biophysics RAS (FSC PSCBS RAS)

Author for correspondence.
Email: tatianabessonova66@gmail.com
Russian Federation, Pushchino, 142290

U. D. Kuznetsova

Pirogov Russian National Research Medical University

Email: tatianabessonova66@gmail.com
Russian Federation, Moscow, 117997

A. T. Magkaev

HSE University

Email: tatianabessonova66@gmail.com
Russian Federation, Moscow, 117418

M. S. Gelfand

Skolkovo Institute of Science and Technology; Institute for Information Transmission Problems RAS

Email: tatianabessonova66@gmail.com
Russian Federation, Moscow, 121205; Moscow, 127051

O. N. Ozoline

Institute of Cell Biophysics RAS (FSC PSCBS RAS)

Email: tatianabessonova66@gmail.com
Russian Federation, Pushchino, 142290

M. N. Tutukina

Institute of Cell Biophysics RAS (FSC PSCBS RAS); Skolkovo Institute of Science and Technology; Institute for Information Transmission Problems RAS

Email: tatianabessonova66@gmail.com
Russian Federation, Pushchino, 142290; Moscow, 121205; Moscow, 127051

References

  1. Bertin P., Terao E., Lee E. H., Lejeune P., Colson C., Danchin A., Collatz E. The H-NS protein is involved in the biogenesis of flagella in Escherichia coli // J. Bacteriol. 1994. V. 176. P. 5537–5540.
  2. Bessonova T. A., Rybina A. A., Marakulina D. A., Kaznadzey A. D., Gelfand M. S., Ozoline O. N., Tutukina M. N. Phylogeny and cross-regulation of the YjjM and LeuO transcription factors translated as multiple protein forms from one gene in Escherichia coli // Math. Biol. Bioinforma. 2023. V. 18. P. 1–14.
  3. Domka J., Lee J., Wood T. K. YliH (BssR) and YceP (BssS) Regulate Escherichia coli K-12 biofilm formation by influencing cell signaling // Appl. Environ. Microbiol. 2006. V. 72. P. 2449–2459.
  4. Fabich A. J., Jones S. A., Chowdhury F. Z., Cernosek A., Anderson A., Smalley D., McHargue J.W., Hightower G. A., Smith J. T., Autieri S. M., Leatham M. P., Lins J. J., Allen R. L., Laux D. C., Cohen P. S., Conway T. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine // Infect. Immun. 2008. V. 76. P. 1143‒1152.
  5. Fuentes D. N., Calderón P. F., Acuña L. G., Rodas P. I., Paredes-Sabja D., Fuentes J. A., Gil F., Calderón I. L. Motility modulation by the small non-coding RNA SroC in Salmonella typhimurium // FEMS Microbiol. Lett. 2015. V. 362. Art. fnv135.
  6. Guadarrama C., Villasenor T., Calva E. The subtleties and contrasts of the LeuO regulator in Salmonella typhi: implications in the immune response // Front. Immunol. 2014. V. 5. Art. 581.
  7. Gudapaty S., Suzuk, K., Wang X., Babitzke P., Romeo T. Regulatory interactions of Csr components: the RNA binding protein CsrA activates csrB transcription in Escherichia coli // J. Bacteriol. 2001. V. 183. P. 6017–6027.
  8. Hammar M., Bian Z., Normark S. Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli // Proc. Natl. Acad. Sci. USA. 1996. V. 93. P. 6562–6566.
  9. Jackson D. W., Suzuki K., Oakford L., Simecka J. W., Hart M. E., Romeo T. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli // J. Bacteriol. 2002. V. 184. P. 290–301.
  10. Jackson D. W., Simecka J. W., Romeo T. Catabolite repression of Escherichia coli biofilm formation // J. Bacteriol. 2002. V. 184. P. 3406–3410.
  11. Jimenez A. G., Ellermann M., Abbott W., Sperandio V. Diet-derived galacturonic acid regulates virulence and intestinal colonization in enterohaemorrhagic Escherichia coli and Citrobacter rodentium // Nat. Microbiol. 2019. V. 5. P. 368–378.
  12. Kaper J. B., Nataro J. P., Mobley H. L.T. Pathogenic Escherichia coli // Nat. Rev. Microbiol. 2004. V. 2. P. 123–140.
  13. Mehta I., Zimmern P., Reitzer L. Enzymatic assay of D-mannose from urine // Bioanalysis. 2018. V. 10. P. 1947‒1954.
  14. Peekhaus N., Conway T. What’s for dinner?: Entner‒Doudoroff metabolism in Escherichia coli // J. Bacteriol. 1998. V. 180. P. 3495‒502.
  15. Pratt L. A., Kolter R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili // Mol. Microbiol. 1998. V. 30. P. 285–293.
  16. Rodrigues D. F., Elimelech M. Role of type 1 fimbriae and mannose in the development of Escherichia coli K12 biofilm: from initial cell adhesion to biofilm formation // Biofouling. 2009. V. 25. P. 401‒411.
  17. Suvorova I. A., Tutukina M. N., Ravcheev D. A., Rodionov D. A., Ozoline O. N., Gelfand M. S. Comparative genomic analysis of the hexuronate metabolism genes and their regulation in gammaproteobacteria // J. Bacteriol. 2011. V. 193. P. 3956‒3963.
  18. Shimada T., Bridier A., Briandet R., Ishihama A. Novel roles of LeuO in transcription regulation of E. coli genome: antagonistic interplay with the universal silencer H-NS // Mol. Microbiol. 2011. V. 82. P. 378‒397.
  19. Tutukina M. N., Potapova A. V., Cole J. A., Ozoline O. N. Control of hexuronate metabolism in Escherichia coli by the two interdependent regulators, ExuR and UxuR: derepression by heterodimer formation // Microbiology (Reading). 2016. V. 162. P. 1220–1231.
  20. Tutukina M. N., Dakhnovets A. I., Kaznadzey A. D., Gelfand M. S., Ozoline O. N. Sense and antisense RNA products of the uxuR gene can affect motility and chemotaxis acting independent of the UxuR protein // Front. Mol. Biosci. 2023. V. 10. Art. 1121376.
  21. Verma R., Rojas T. C.G., Maluta R. P., Leite J. L., Da Silva L. P.M., Nakazato G., Dias Da Silveira W. Fimbria-encoding gene yadC has a pleiotropic effect on several biological characteristics and plays a role in avian pathogenic Escherichia coli pathogenicity // Infect. Immun. 2016. V. 84. P. 187–193.
  22. Wood T. K., González Barrios A. F., Herzberg M., Lee J. Motility influences biofilm architecture in Escherichia coli // Appl. Microbiol. Biotechnol. 2006. V. 72. P. 361–367.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. a – Assessment of the effect of removal of leuO, uxuR, crp, exuR, yjjM on the adhesion of E. coli K-12 to cells of the intestinal epithelium CaCo-2; b – mobility of E. coli K-12 cells in 0.3% LB agar; c – adhesion of E. coli K-12 MG1655 and E. coli Nissle 1917 to CaCo-2 cells in the presence of 0.2% D-galacturonate, D-glucuronate or D-mannose.

Download (193KB)
Indexing metadata
3. Fig. 2. a – Formation of biofilms (data on three tablets in one experiment). The strains are described in the legend; b – the effect of the carbon source on the efficiency of biofilm formation of E. coli K-12 MG1655 and E. coli Nissle 1917; c ‒ a diagram of the uxuR gene sites deleted in E. coli K-12 MG1655 ΔuxuR and ΔuxuR_tr strains. PlatProm scores are deposited along the ordinate axis, reflecting the probability of transcription initiation at a specific point. The site of synthesis of regulatory RNAs is highlighted in pink; g is the dynamics of expression of the csgD, fliA and csrC genes in E. coli K-12 MG1655 upon removal of uxuR, crp and yjjM.

Download (264KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences