1887

Abstract

A marine strain of capable of activating multiple acylated homoserine lactone (AHL)-based reporter cultures was isolated. The cognate signal molecule was characterized as octanoyl homoserine lactone (OHL) and its production was observed to be growth dependent, with maximum production (5.675 µg l) at 24 h growth. The strain exhibited swarming, but its motility was not affected upon addition of pure OHL or culture supernatant. Phytochemicals such as quercitin and berberine chloride inhibited OHL production and reduced swarming. FliA, the predominantly upregulated protein during swarming, was considered as a possible target for these inhibitors, and docking of the two most active and two least active inhibitors to this protein suggested preferential binding of the former set of compounds. Apart from adding new evidence to AHL production in , active inhibitors shortlisted from this study could help in identifying lead compounds to act against this opportunistic pathogen of the respiratory and gastrointestinal tract.

Funding
This study was supported by the:
  • Council of Scientific and Industrial Research
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.080838-0
2014-10-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/10/2170.html?itemId=/content/journal/micro/10.1099/mic.0.080838-0&mimeType=html&fmt=ahah

References

  1. Armbruster C. E., Mobley H. L. T. ( 2012). Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis. Nat Rev Microbiol 10:743–754 [View Article][PubMed]
    [Google Scholar]
  2. Biswa P., Doble M. ( 2013). Production of acylated homoserine lactone by Gram-positive bacteria isolated from marine water. FEMS Microbiol Lett 343:34–41 [View Article][PubMed]
    [Google Scholar]
  3. Borges A., Serra S., Cristina Abreu A., Saavedra M. J., Salgado A., Simoes M. ( 2014). Evaluation of the effects of selected phytochemicals on quorum sensing inhibition and in vitro cytotoxicity. Biofouling 30:183–195 [View Article][PubMed]
    [Google Scholar]
  4. Bruhn J. B., Christensen A. B., Flodgaard L. R., Nielsen K. F., Larsen T. O., Givskov M., Gram L. ( 2004). Presence of acylated homoserine lactones (AHLs) and AHL-producing bacteria in meat and potential role of AHL in spoilage of meat. Appl Environ Microbiol 70:4293–4302 [View Article][PubMed]
    [Google Scholar]
  5. Caiazza N. C., Merritt J. H., Brothers K. M., O’Toole G. A. ( 2007). Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:3603–3612 [View Article][PubMed]
    [Google Scholar]
  6. Charlton T. S., de Nys R., Netting A., Kumar N., Hentzer M., Givskov M., Kjelleberg S. ( 2000). A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ Microbiol 2:530–541 [View Article][PubMed]
    [Google Scholar]
  7. Christensen G. D., Simpson W. A., Younger J. J., Baddour L. M., Barrett F. F., Melton D. M., Beachey E. H. ( 1985). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22:996–1006[PubMed]
    [Google Scholar]
  8. Clarke M. B., Sperandio V. ( 2005). Transcriptional regulation of flhDC by QseBC and σ (FliA) in enterohaemorrhagic Escherichia coli. Mol Microbiol 57:1734–1749 [View Article][PubMed]
    [Google Scholar]
  9. Czerwonka G., Arabski, M., Jabłońska-Wawrzycka A., Rogala P., Kaca W. ( 2014). Morphological changes in Proteus mirabilis O18 biofilm under the influence of a urease inhibitor and a homoserine lactone derivative. Arch Microbiol 196:1–8 [View Article][PubMed]
    [Google Scholar]
  10. Daniels R., Vanderleyden J., Michiels J. ( 2004). Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 28:261–289 [View Article][PubMed]
    [Google Scholar]
  11. Decho A. W., Frey R. L., Ferry J. L. ( 2011). Chemical challenges to bacterial AHL signaling in the environment. Chem Rev 111:86–99 [View Article][PubMed]
    [Google Scholar]
  12. Ding L., Wang Y., Hu Y., Atkinson S., Williams P., Chen S. ( 2009). Functional characterization of FlgM in the regulation of flagellar synthesis and motility in Yersinia pseudotuberculosis. Microbiology 155:1890–1900 [View Article][PubMed]
    [Google Scholar]
  13. Dobretsov S., Teplitski M., Paul V. ( 2009). Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25:413–427 [View Article][PubMed]
    [Google Scholar]
  14. Gram L., de Nys R., Maximilien R., Givskov M., Steinberg P., Kjelleberg S. ( 1996). Inhibitory effects of secondary metabolites from the red alga Delisea pulchra on swarming motility of Proteus mirabilis. Appl Environ Microbiol 62:4284–4287[PubMed]
    [Google Scholar]
  15. Gul N., Ozkorkmaz E. G., Kelesoglu I., Ozluk A. ( 2013). An ultrastructural study, effects of Proteus vulgaris OX19 on the rabbit spleen cells. Micron 44:133–136 [View Article][PubMed]
    [Google Scholar]
  16. Holden M. T. G., Ram Chhabra S., de Nys R., Stead P., Bainton N. J., Hill P. J., Manefield M., Kumar N., Labatte M. & other authors ( 1999). Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol Microbiol 33:1254–1266 [View Article][PubMed]
    [Google Scholar]
  17. Jones B. V., Young R., Mahenthiralingam E., Stickler D. J. ( 2004). Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection. Infect Immun 72:3941–3950 [View Article][PubMed]
    [Google Scholar]
  18. Jones S. M., Dang T. T., Martinuzzi R. ( 2009). Use of quorum sensing antagonists to deter the formation of crystalline Proteus mirabilis biofilms. Int J Antimicrob Agents 34:360–364 [View Article][PubMed]
    [Google Scholar]
  19. Kalia V. C. ( 2013). Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245 [View Article][PubMed]
    [Google Scholar]
  20. Kamatkar N. G., Shrout J. D. ( 2011). Surface hardness impairment of quorum sensing and swarming for Pseudomonas aeruginosa. PLoS ONE 6:e20888 [View Article][PubMed]
    [Google Scholar]
  21. Manos J., Belas R. ( 2006). The genera Proteus, Providencia, and Morganella. The Prokaryotes 6:245–269 [View Article]
    [Google Scholar]
  22. Montgomery K., Charlesworth J. C., LeBard R., Visscher P. T., Burns B. P. ( 2013). Quorum sensing in extreme environments. Life 3:131–148 [View Article]
    [Google Scholar]
  23. Morin D., Grasland B., Vallée-Réhel K., Dufau C., Haras D. ( 2003). On-line high-performance liquid chromatography-mass spectrometric detection and quantification of N-acylhomoserine lactones, quorum sensing signal molecules, in the presence of biological matrices. J Chromatogr A 1002:79–92 [View Article][PubMed]
    [Google Scholar]
  24. Nazzaro F., Fratianni F., Coppola R. ( 2013). Quorum sensing and phytochemicals. Int J Mol Sci 14:12607–12619 [View Article][PubMed]
    [Google Scholar]
  25. Ng W. L., Bassler B. L. ( 2009). Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222 [View Article][PubMed]
    [Google Scholar]
  26. O’Hara C. M., Brenner F. W., Miller J. M. ( 2000). Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev 13:534–546 [View Article][PubMed]
    [Google Scholar]
  27. Ollivier B., Caumette P., Garcia J.-L., Mah R. A. ( 1994). Anaerobic bacteria from hypersaline environments. Microbiol Rev 58:27–38[PubMed]
    [Google Scholar]
  28. Packiavathy I. A. S. V., Sasikumar P., Pandian S. K., Veera Ravi A. ( 2013). Prevention of quorum-sensing-mediated biofilm development and virulence factors production in Vibrio spp. by curcumin. Appl Microbiol Biotechnol 97:10177–10187 [View Article][PubMed]
    [Google Scholar]
  29. Palomino J.-C., Martin A., Camacho M., Guerra H., Swings J., Portaels F. ( 2002). Resazurin microtiter assay plate: simple and inexpensive method for detection of drug resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 46:2720–2722 [View Article][PubMed]
    [Google Scholar]
  30. Pandey J. K., Narayan A., Tyagi S. ( 2013). Prevalence of Proteus species in clinical samples, antibiotic sensitivity pattern and ESBL production. Int. J. Curr. Microbiol. App. Sci 2:253–261
    [Google Scholar]
  31. Pearson M. M., Rasko D. A., Smith S. N., Mobley H. L. T. ( 2010). Transcriptome of swarming Proteus mirabilis. Infect Immun 78:2834–2845 [View Article][PubMed]
    [Google Scholar]
  32. Sarker S. D., Nahar L., Kumarasamy Y. ( 2007). Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42:321–324 [View Article][PubMed]
    [Google Scholar]
  33. Sorenson M. K., Ray S. S., Darst S. A. ( 2004). Crystal structure of the flagellar σ/anti-σ complex σ28/FlgM reveals an intact σ factor in an inactive conformation. Mol Cell 14:127–138 [View Article][PubMed]
    [Google Scholar]
  34. Stankowska D., Kwinkowski M., Kaca W. ( 2008). Quantification of Proteus mirabilis virulence factors and modulation by acylated homoserine lactones. J Microbiol Immunol Infect 41:243–253[PubMed]
    [Google Scholar]
  35. Stankowska D., Czerwonka G., Rozalska S., Grosicka M., Dziadek J., Kaca W. ( 2012). Influence of quorum sensing signal molecules on biofilm formation in Proteus mirabilis O18. Folia Microbiol (Praha) 57:53–60 [View Article][PubMed]
    [Google Scholar]
  36. Steidle A., Allesen-Holm M., Riedel K., Berg G., Givskov M., Molin S., Eberl L. ( 2002). Identification and characterization of an N-acylhomoserine lactone-dependent quorum-sensing system in Pseudomonas putida strain IsoF. Appl Environ Microbiol 68:6371–6382 [View Article][PubMed]
    [Google Scholar]
  37. Teplitski M., Eberhard A., Gronquist M. R., Gao M., Robinson J. B., Bauer W. D. ( 2003). Chemical identification of N-acyl homoserine lactone quorum-sensing signals produced by Sinorhizobium meliloti strains in defined medium. Arch Microbiol 180:494–497 [View Article][PubMed]
    [Google Scholar]
  38. Vattem D. A., Mihalik K., Crixell S. H., McLean R. J. C. ( 2007). Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78:302–310 [View Article][PubMed]
    [Google Scholar]
  39. Vikram A., Jayaprakasha G. K., Jesudhasan P. R., Pillai S. D., Patil B. S. ( 2010). Suppression of bacterial cell–cell signalling, biofilm formation and type III secretion system by citrus flavonoids. J Appl Microbiol 109:515–527[PubMed]
    [Google Scholar]
  40. Wang W.-B., Lai H.-C., Hsueh P.-R., Chiou R. Y. Y., Lin S.-B., Liaw S.-J. ( 2006). Inhibition of swarming and virulence factor expression in Proteus mirabilis by resveratrol. J Med Microbiol 55:1313–1321 [View Article][PubMed]
    [Google Scholar]
  41. Yah S. C., Eghafona N. O., Oranusi S., Abouo A. M. ( 2007). Widespread plasmid resistance genes among Proteus species in diabetic wounds of patients in the Ahmadu Bello University Teaching Hospital (ABUTH) Zaria. Afr J Biotechnol 6:
    [Google Scholar]
  42. Zhao J. Y., Dang H. ( 2012). Coastal seawater bacteria harbor a large reservoir of plasmid-mediated quinolone resistance determinants in Jiaozhou Bay, China. Microb Ecol 64:187–199 [View Article][PubMed]
    [Google Scholar]
  43. Zhou L., Zheng H., Tang Y., Yu W., Gong Q. ( 2013). Eugenol inhibits quorum sensing at sub-inhibitory concentrations. Biotechnol Lett 35:631–637 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.080838-0
Loading
/content/journal/micro/10.1099/mic.0.080838-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

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