Abstract
In order to control the clonal population’s fitness to manage the expense of the resources by the community, it is not surprising that bacterial communities coordinate the formation of persister cells (bacterial subpopulations that survive stress conditions such as antibiotic or environmental threats). The development of these persister cells is linked to the activity of intercellular signaling molecules. Among them, we focus on acyl-homoserine lactone (AHL), the competence-stimulating peptide (CSP), indole (IND) and autoinducer-2 (AI-2), all involved in the quorum sensing systems activation in several pathogens. In this work, we will describe the action of these molecules related with quorum sensing systems in Gram positive Streptococcus mutans and Staphylococcus aureus and in Gram negative Pseudomonas aeruginosa, Escherichia coli, and Acinetobacter spp. bacteria.
Keywords
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Leung, V., & Lévesque, C. M. (2012). A stress-inducible quorum-sensing peptide mediates the formation of persister cells with noninherited multidrug tolerance. Journal of Bacteriology, 194, 2265–2274.
Wood, T. K. (2016). Combatting bacterial persister cells. Biotechnology and Bioengineering, 113, 476–483.
Hobby, G. L., Meyer, K., & Chaffee, E. (1942). Observations on the mechanism of action of penicillin. Experimental Biology and Medicine, 50, 281–285.
Bigger, J. (1994). Treatment of staphylococcal infections with penicillin by intermittent sterilisation. The Lancet, 244, 497–500.
Costerton, J. W., Stewart, P. S., & Greenberg, E. P. (1999). Bacterial biofilms: A common cause of persistent infections. Science, 284, 1318–1322.
Harrison, J. J., Turner, R. J., & Ceri, H. (2005). Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginosa. Environmental Microbiology, 7, 981–994.
Lewis, K. (2010). Persister cells. Annual Review of Microbiology, 64, 357–372.
Cohen, N. R., Lobritz, M. A., & Collins, J. J. (2013). Microbial persistence and the road to drug resistance. Cell Host & Microbe, 13, 632–642.
Maisonneuve, E., & Gerdes, K. (2014). Molecular mechanisms underlying bacterial persisters. Cell, 157, 539–548.
Harms, A., Maisonneuve, E., Gerdes, K. (2016). Mechanisms of bacterial persistence during stress and antibiotic exposure. Science, 16(354), 6318.
Hong, S. H., Wang, X., O’Connor, H. F., Benedik, M. J., & Wood, T. K. (2012). Bacterial persistence increases as environmental fitness decreases. Microbial Biotechnology, 5(4), 509–522.
Moyed, H. S., & Bertrand, K. P. (1983). hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. Journal of Bacteriology, 155, 768–775.
Kim, Y., & Wood, T. K. (2010). Toxins Hha and CspD and small RNA regulator Hfq are involved in persister cell formation through MqsR in Escherichia coli. Biochemical and Biophysical Research Communications, 391, 209–213.
Luidalepp, H., Jõers, A., Kaldalu, N., & Tenson, T. (2011). Age of inoculum strongly influences persister frequency and can mask effects of mutations implicated in altered persistence. Journal of Bacteriology, 193, 3598–3605.
Dörr, T., Vulić, M., & Lewis, K. (2010). Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biology, 8, e1000317.
Harrison, J. J., Wade, W. D., Akierman, S., Vacchi-Suzzi, C., Stremick, C. A., Turner, R. J., & Ceri, H. (2009). The chromosomal toxin gene yafQ is a determinant of multidrug tolerance for Escherichia coli growing in a biofilm. Antimicrobial Agents and Chemotherapy, 53, 2253–2258.
Page, R., & Peti, W. (2016). Toxin-antitoxin systems in bacterial growth arrest and persistence. Nature Chemical Biology, 12, 208–214.
Kim, J.-S., & Wood, T. K. (2016). Persistent persister misperceptions. Frontiers in Microbiology, 7, 2134.
Harms, A., Fino, C., Sørensen, M. A., Semsey, S., & Gerdes, K. (2017). Prophages and growth dynamics confound experimental results with antibiotic-tolerant persister cells. MBio, 8, e01964–e01917.
Fauvart, M., De Groote, V. N., & Michiels, J. (2011). Role of persister cells in chronic infections: Clinical relevance and perspectives on anti-persister therapies. Journal of Medical Microbiology, 60, 699–709.
Chowdhury, N., Kwan, B. W., Wood, T. K. (2016). Persistence increases in the absence of the alarmone guanosine tetraphosphate by reducing cell growth. Scientific Reports 6, 20519.
Taga, M. E., & Bassler, B. L. (2003). Chemical communication among bacteria. Proceedings of the National Academy of Sciences of the United States of America, 100(Suppl 2), 14549–14554.
Lee, J., Bansal, T., Jayaraman, A., Bentley, W. E., & Wood, T. K. (2007). Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Applied and Environmental Microbiology, 73, 4100–4109.
Fuqua, W. C., Winans, S. C., & Greenberg, E. P. (1994). Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. Journal of Bacteriology, 176, 269–275.
Salmond, G. P. C., Bycroft, B. W., Stewart, G. S. A. B., & Williams, P. (1995). The bacterial ‘enigma’: Cracking the code of cell-cell communication. Molecular Microbiology, 16, 615–624.
Li, Y.-H., Tang, N., Aspiras, M. B., Lau, P. C. Y., Lee, J. H., Ellen, R. P., & Cvitkovitch, D. G. (2002). A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. Journal of Bacteriology, 184, 2699–2708.
Perry, J. A., Jones, M. B., Peterson, S. N., Cvitkovitch, D. G., & Lévesque, C. M. (2009). Peptide alarmone signalling triggers an auto-active bacteriocin necessary for genetic competence. Molecular Microbiology, 72, 905–917.
Dufour, D., Cordova, M., Cvitkovitch, D. G., & Lévesque, C. M. (2011). Regulation of the competence pathway as a novel role associated with a streptococcal bacteriocin. Journal of Bacteriology, 193, 6552–6559.
Leung, V., Ajdic, D., Koyanagi, S., & Lévesque, C. M. (2015). The formation of Streptococcus mutans persisters induced by the quorum-sensing peptide pheromone is affected by the LexA regulator. Journal of Bacteriology, 197, 1083–1094.
Leung, V., Dufour, D., & Lévesque, C. M. (2015). Death and survival in Streptococcus mutans: Differing outcomes of a quorum-sensing signaling peptide. Frontiers in Microbiology, 6, 1176.
Lee, J., Zhang, X.-S., Hegde, M., Bentley, W. E., Jayaraman, A., & Wood, T. K. (2008). Indole cell signaling occurs primarily at low temperatures in Escherichia coli. The ISME Journal, 2, 1007–1023.
Shimada, Y., Kinoshita, M., Harada, K., Mizutani, M., Masahata, K., Kayama, H., & Takeda, K. (2013). Commensal bacteria-dependent indole production enhances epithelial barrier function in the colon. PLoS One, 8, e80604.
Bansal, T., Alaniz, R. C., Wood, T. K., & Jayaraman, A. (2010). The bacterial signal indole promotes epithelial cell barrier properties and attenuates inflammation. PNAS, 107, 228–233.
Lee, J., Jayaraman, A., & Wood, T. K. (2007). Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiology, 7, 42.
Lee, J., Attila, C., Cirillo, S. L., Cirillo, J. D., & Wood, T. K. (2009). Indole and 7-hydoxyindole diminish Pseudomonas aeruginosa virulence. Microbial Biotechnology, 2, 75–90.
Lee, J. H., Wood, T. K., & Lee, J. (2015). Roles of indole as an interspecies and interkingdom signaling molecule. Trends in Microbiology, 23, 707–718.
Vega, N. M., Allison, K. R., Khalil, A. S., & Collins, J. J. (2012). Signaling-mediated bacterial persister formation. Nature Chemical Biology, 8, 431–433.
Hirakawa, H., Inazumi, Y., Masaki, T., Hirata, T., & Yamaguchi, A. (2005). Indole induces the expression of multidrug exporter genes in Escherichia coli. Molecular Microbiology, 55, 1113–1126.
Li, X., Yang, Q., Dierckens, K., Milton, D. L., & Defoirdt, T. (2014). RpoS and indole signaling control the virulence of Vibrio anguillarum towards gnotobiotic sea bass (Dicentrarchus labrax) larvae. PLoS One, 9, e111801.
Chu, W., Zere, T. R., Weber, M. M., Wood, T. K., Whiteley, M., Hidalgo-Romano, B., Valenzuela, E., & McLean, R. J. (2012). Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling. Applied and Environmental Microbiology, 78, 411–419.
Vega, N. M., Allison, K. R., Samuels, A. N., Klempner, M. S., & Collins, J. J. (2013). Salmonella typhimurium intercepts Escherichia coli signaling to enhance antibiotic tolerance. Proceedings of the National Academy of Sciences of the United States of America, 110, 14420–14425.
Kim, J., & Park, W. (2013). Indole inhibits bacterial quorum sensing signal transmission by interfering with quorum sensing regulator folding. Microbiology, 159, 2616–2625.
Kim, J., & Park, W. (2015). Indole: A signaling molecule or a mere metabolic byproduct that alters bacterial physiology at a high concentration? Journal of Microbiology, 53, 421–428.
Wang, Y., Li, H., Cui, X., & Zhang, X. H. (2017). A novel stress response mechanism, triggered by indole, involved in quorum quenching enzyme MomL and iron-sulfur cluster in Muricauda olearia Th120. Scientific Reports, 7, 4252.
Chen, X., Schauder, S., Potier, N., Av, D., Pelczer, I., Bassler, B. L., & Hughson, F. M. (2002). Structural identification of a bacterial quorum-sensing signal containing boron. Nature, 415, 545–549.
Camilli, A., & Bassler, B. L. (2006). Bacterial small-molecule signaling pathways. Science, 311, 1113–1116.
Waters, C. M., & Bassler, B. L. (2005). Quorum sensing: Cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology, 21, 319–346.
Schauder, S., Shokat, K., Surette, M. G., & Bassler, B. L. (2001). The LuxS-family of bacterial autoinducers: Biosynthesis of a novel quorum-sensing signal molecule. Molecular Microbiology, 41, 463–476.
Herzberg, M., Kaye, I. K., Peti, W., & Wood, T. K. (2006). YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 by enhancing autoinducer 2 transport. Journal of Bacteriology, 188, 587–598.
González Barrios, A. F., Zuo, R., Hashimoto, Y., Yang, L., Bentley, W. E., & Wood, T. K. (2006). Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). Journal of Bacteriology, 188, 305–316.
Kwan, B. W., Osbourne, D. O., Hu, Y., Benedik, M. J., & Wood, T. K. (2015). Phosphodiesterase DosP increases persistence by reducing cAMP which reduces the signal indole. Biotechnology and Bioengineering, 112, 588–600.
Hu, Y., Kwan, B. W., Osbourne, D. O., Benedik, M. J., & Wood, T. K. (2015). Toxin YafQ increases persister cell formation by reducing indole signalling. Environmental Microbiology, 17, 1275–1285.
Lee, J. H., Kim, Y. G., Gwon, G., Wood, T. K., & Lee, J. (2016). Halogenated indoles eradicate bacterial persister cells and biofilms. AMB Express, 6, 123.
Ren, D., Sims, J. J., & Wood, T. K. (2001). Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2-(5H)-furanone. Environmental Microbiology, 3, 731–736.
Pan, J., Bahar, A. A., Syed, H., & Ren, D. (2012). Reverting antibiotic tolerance of Pseudomonas aeruginosa PAO1 persister cells by (Z)-4-bromo-5-(bromomethylene)-3-methylfuran-2(5H)-one. PLoS One, 7, e45778.
Pan, J., Song, F., & Ren, D. (2013). Controlling persister cells of Pseudomonas aeruginosa PDO300 by (Z)-4-bromo-5-(bromomethylene)-3-methylfuran-2(5H)-one. Bioorganic & Medicinal Chemistry Letters, 23, 4648–4651.
Pan, J., Xie, X., Tian, W., Bahar, A. A., Lin, N., Song, F., An, J., & Ren, D. (2013). (Z)-4-bromo-5-(bromomethylene)-3-methylfuran-2(5H)-one sensitizes Escherichia coli persister cells to antibiotics. Applied Microbiology and Biotechnology, 97, 9145–9154.
Möker, N., Dean, C. R., & Tao, J. (2010). Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorum-sensing signaling molecules. Journal of Bacteriology, 192, 1946–1955.
Allegretta, G., Maurer, C. K., Eberhard, J., Maura, D., Hartmann, R. W., Rahme, L., & Empting, M. (2017). In-depth profiling of MvfR-regulated small molecules in Pseudomonas aeruginosa after quorum sensing inhibitor treatment. Frontiers in Microbiology, 8, 924.
Que, Y. A., Hazan, R., Strobel, B., Maura, D., He, J., Kesarwani, M., Panopoulos, P., Tsurumi, A., Giddey, M., Wilhelmy, J., Mindrinos, M. N., & Rahme, L. G. (2013). A quorum sensing small volatile molecule promotes antibiotic tolerance in bacteria. PLoS One, 8, e80140.
Cheng, H.-Y., Soo, V. W. C., Islam, S., McAnulty, M. J., Benedik, M. J., & Wood, T. K. (2014). Toxin GhoT of the GhoT/GhoS toxin/antitoxin system damages the cell membrane to reduce adenosine triphosphate and to reduce growth under stress. Environmental Microbiology, 16, 1741–1754.
Conlon, B. P., Rowe, S. E., Gandt, A. B., Nuxoll, A. S., Donegan, N. P., Zalis, E. A., Clair, G., Adkins, J. N., Cheung, A. L., & Lewis, K. (2016). Persister formation in Staphylococcus aureus is associated with ATP depletion. Nature Microbiology, 1, 16051.
Shan, Y., Brown Gandt, A., Rowe, S. E., Deisinger, J. P., Conlon, B. P., & Lewis, K. (2017). ATP-dependent persister formation in Escherichia coli. MBio, 8, e02267–e02216.
Xu, T., Wang, X.-Y., Cui, P., Zhang, Y.-M., Zhang, W.-H., & Zhang, Y. (2017). The Agr quorum sensing system represses persister formation through regulation of phenol soluble modulins in Staphylococcus aureus. Frontiers in Microbiology, 8, 2189.
Acknowledgements
We thank the financing by grants PI13/02390 and PI16/01163 awarded to M. Tomás within the State Plan for R+D+I 2013–2016 (National Plan for Scientific Research, Technological Development and Innovation 2008–2011) and co-financed by the ISCIII-Deputy General Directorate of evaluation and Promotion of Research-European Regional Development Fund “A way of Making Europe” and Instituto de Salud Carlos III FEDER. M.Tomás was financially supported by the Miguel Servet Research Programme (SERGAS and ISCIII). L. Fernández-García was financially supported by a predoctoral fellowship from the Xunta de Galicia (GAIN, Axencia de Innovación). Finally, we would to thank to Spanish Network for Research in Infectious Diseases (REIPI), Spain (RD12/0015/0010, RD16/0016/0001 and RD16/0016/0006).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Fernandez-García, L., Blasco, L., Trastoy, R., García-Contreras, R., Wood, T.K., Tomás, M. (2018). Quorum Sensing Systems and Persistence. In: Pallaval Veera Bramhachari (eds) Implication of Quorum Sensing System in Biofilm Formation and Virulence. Springer, Singapore. https://doi.org/10.1007/978-981-13-2429-1_3
Download citation
DOI: https://doi.org/10.1007/978-981-13-2429-1_3
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-13-2428-4
Online ISBN: 978-981-13-2429-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)