Abstract
The goal of the work was to analyze the ability of natural and semisynthetic penicillins to regulate the quorum sensing system in bacteria. The test strain was C. violaceum NCTC 13274 (CV 026) bearing mini-Tn5 insertion in the cviI gene that led to irreversible loss of N-acyl-L-homoserine lactone (AHL) biosynthesis and reversible suppression of violacein biosynthesis. Within the temperature range suboptimal for C. violaceum growth (17–22°C), subinhibitory concentrations of piperacillin, azlocillin, ticarcillin, carbenicillin, and oxacillin showed a quorum-dependent induction of violacein production, probably acting as AHL-mimetics. Cleavage of these antibiotics with beta-lactamase I and II led to the loss of both antibacterial and quorum-inducing activities. Inhibition of C. violaceum beta-lactamase by sulbactam resulted in manifestation of combined antibacterial and quorum-inducing activity of ampicillin and amoxicillin. These results improve our understanding of the role of beta-lactams and beta-lactamases in the processes of interspecific antagonism and in microbial intercellular communication.
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References
Aminov, R.I., A brief history of the antibiotic era: lessons learned and challenges for the future, Front. Microbiol., 2010, vol. 1, p. 134.
Andrew, J.C., The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability, Braz. Natl. Genome Project Consortium, 2003, vol. 100, pp. 116–125.
Blosser, R.S. and Gray, K.M., Extraction of violacein from Chromobacterium violaceum provides a new quantitative bioassay for N-acyl homoserine lactone autoinducers, J. Microbiol. Methods, 2000, vol. 40, pp. 47–55.
Brumback, K.C., Eason, B.D., and Anderson, L.K., The Serratia-type hemolysin of Chromobacterium violaceum, FEMS Microbiol. Lett., 2007, vol. 267, pp. 243–250.
Bulgakova, V.G., Vinogradova, K.A., Orlova, T.I., Kozhevin, P.A., and Polin, A.N., Action of antibiotics as signal molecules, Antibiot. Khimioterap., 2014, vol. 1, pp. 36–43.
Calabrese, E.J., The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: an overview, Toxicol. Appl. Pharmacol., 2005, vol. 202, pp. 289–301.
Fantinatti-Garboggini, F., Almeida, Rd., Portillo, Vdo A., Barbosa, T.A., Trevilato, P.B., Neto, C.E., Trevilato, P.B., Neto, C.E., Coêlho, R.D., Silva, D.W., Bartoleti, L.A., Hanna, E.S., Brocchi, M., and Manfio, G.P., Drug resistance in Chromobacterium violaceum, Genet. Mol. Res., 2004, vol. 31, no. 3, pp. 134–147.
Farrar, W.E., Jr. and O’dell, N.M., Beta-lactamase activity in Chromobacterium violaceum, J. Infect. Dis., 1976, vol. 134, pp. 290–293.
Garske, L.A., Beatson, S.A., Leech, A.J., Walsh, S.L., and Bell, S.C., Sub-inhibitory concentrations of ceftazidime and tobramycin reduce the quorum sensing signals of Pseudomonas aeruginosa, Pathology, 2004, vol. 36, pp. 571–575.
Kozhevin, P.A., Natural functions of antibiotics as informbiotics, Bull. Mos. Gos. Univ., Ser. 17, Soil Sci., 2014, vol. 3, pp. 3–9.
Kumar, M.R., Chromobacterium violaceum: a rare bacterium isolated from a wound over the scalp, Int. J. Appl. Basic. Med. Res., 2012, vol. 2, no. 1, pp. 70–72.
Lee, J., Kim, S., Nahm, C.H., Choi, J.W., Kim, J., Pai, S.H., Moon, K.H., Lee, K., and Chong, Y., Two cases of Chromobacterium violaceum infection after injury in a subtropical region, J. Clin. Microbiol., 1999, vol. 37, pp. 2068–2070.
Linares, J.F., Gustafsson, I., Baquero, F., and Martinez, J.L., Antibiotics as intermicrobial signaling agents instead of weapons, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 19484–19489.
Liu, Z., Wang, W., Zhu, Y., Gong, Q., Yu, W., and Lu, X., Antibiotics at subinhibitory concentrations improve the quorum sensing behavior of Chromobacterium violaceum, FEMS Microbiol. Lett., 2013, vol. 341, pp. 37–44.
Manukhov, I.V., Melkina, O.E., Goryanin, I.I., Baranova, A.V., and Zavilgelsky, G.B., The N-terminal domain of Aliivibrio fischeri LuxR is a target of the GroEL chaperonin, J. Bacteriol., 2010, vol. 192, pp. 5549–5551.
Mukherji, R. and Prabhune, A., A rapid iodometric method for qualitative detection of AHL lactonases, World J. Pharm. Res., 2013, vol. 3, pp. 1126–1132.
Shen, L., Shi, Y., Zhang, D., Wei, J., Surette, M.G., and Duan, K., Modulation of secreted virulence factor genes by subinhibitory concentrations of antibiotics in Pseudomonas aeruginosa, J. Microbiol., 2008, vol. 46, pp. 441–447.
Skindersoe, M.E., Alhede, M., Phipps, R., Yang, L., Jensen, P.O., Rasmussen, T.B., Bjarnsholt, T., Tolker-Nielsen, T., Høiby, N., and Givskov, M., Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa, Antimicrob. Agents Chemother., 2008, vol. 52, pp. 3648–3663.
Stauff, D.L. and Bassler, B.L., Quorum sensing in Chromobacterium violaceum: DNA recognition and gene regulation by the CviR receptor, J. Bacteriol., 2011, vol. 193, pp. 3871–3878.
Swain, B., Otta, S., Sahu, K.K., Panda, K., and Rout, S., Urinary tract infection by Chromobacterium violaceum, J. Clin. Diagn. Res., 2014, vol. 8, no. 8, pp. 1–2.
Tang, K. and Zhang, X., Quorum quenching agents: resources for antivirulence therapy, Mar. Drugs, 2014, vol. 12, pp. 3245–3282.
Wai-Leung, N. and Bassler, B.L., Bacterial quorum sensing network architectures, Annu. Rev. Genet., 2009, vol. 43, pp. 197–222.
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Original Russian Text © D.G. Deryabin, K.S. Inchagova, 2017, published in Mikrobiologiya, 2017, Vol. 86, No. 4, pp. 448–454.
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Deryabin, D.G., Inchagova, K.S. Subinhibitory concentrations of the penicillin antibiotics induce quorum-dependent violacein synthesis in Chromobacterium violaceum . Microbiology 86, 463–468 (2017). https://doi.org/10.1134/S0026261717040051
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DOI: https://doi.org/10.1134/S0026261717040051