Peculiarities of Staphylococci and Streptococci Communication in Biofilms
DOI:
https://doi.org/10.15407/Keywords:
quorum sensing, biofilm, Staphylococcus, Streptococcus, virulence factors, antimicrobial resistanceAbstract
Aim. To summarize and systematize many years of research on the communication mechanisms (quorum sensing) of biofilm representatives such as staphylococci and streptococci, and to analyze the genetic predictors of virulence property changes in these bacteria. Methods. A systematic search and analysis of scientific literature were conducted using the PubMed, Scopus, and Google Scholar databases. The review focuses on the molecular and genetic mechanisms of Quorum Sensing systems (Agr, LuxS, Fsr, Rgg) in Gram-positive cocci and their role in biofilm formation on biotic and abiotic surfaces. Results. The role of the Agr and LuxS regulatory systems of cocci in the expression of genes responsible for the synthesis of virulence factors such as toxins, enzymes, and factors that suppress the host immune response is described. It has been confirmed that the effect of Agr on biofilm-associated infection varies: Agr is necessary for biofilm structuring and the spread of infection, but Agr dysfunction leads to enhanced biofilm formation, which may be beneficial for bacteria under chronic conditions. Additionally, the mechanisms of antimicrobial resistance gene expression under the regulatory influence of QS are revealed. Conclusions. The review highlights the possibility of influencing the development of virulence properties of opportunistic microorganisms and their antimicrobial resistance through innovative non-bactericidal therapeutic strategies. This opens a new page in the fight against multidrug-resistant pathogens of nosocomial infections and the correction of the microbiome in general.
Downloads
References
Alonzo III, F., & Torres, V. J. (2014). The bicomponent pore-forming leucocidins of Staphylococcus aureus. Microbiology and Molecular Biology Reviews, 78(2), 199-230. https://doi.org/10.1128/MMBR.00055-13
Alonzo III, F., Benson, M. A., Chen, J., Novick, R. P., Shopsin, B., & Torres, V. J. (2012). Staphylococcus aureus leucocidin ED contributes to systemic infection by targeting neutrophils and promoting bacterial growth in vivo. Molecular Microbiology, 83(2), 423-435. https://doi.org/10.1111/j.1365-2958.2011.07942.x
Alonzo III, F., Kozhaya, L., Rawlings, S. A., Reyes-Robles, T., DuMont, A. L., Myszka, D. G., Landau, N. R., Unutmaz, D., & Torres, V. J. (2013). CCR5 is a receptor for Staphylococcus aureus leukotoxin ED. Nature, 493(7430), 51-55. https://doi.org/10.1038/nature11724
Anbalagan, S., McShan, W. M., Dunman, P. M., & Chaussee, M. S. (2011). Identification of Rgg binding sites in the Streptococcus pyogenes chromosome. Journal of Bacteriology, 193(18), 4933-4942. https://doi.org/10.1128/JB.00429-11
Bassler, B. L. (2002). Small talk: cell-to-cell communication in bacteria. Cell, 109(4), 421-424. https://doi.org/10.1016/S0092-8674(02)00749-3
Becker, S., Frankel, M. B., Schneewind, O., & Missiakas, D. (2014). Release of protein A from the cell wall of Staphylococcus aureus. Proceedings of the National Academy of Sciences, 111(4), 1574-1579. https://doi.org/10.1073/pnas.1317181111
Belman, S., Lefrancq, N., Nzenze, S., Downs, S., du Plessis, M., Lo, S. W., Global Pneumococcal Sequencing Consortium, McGee, L., Madhi, S. A., von Gottberg, A., Bentley, S. D., & Salje, H. (2024). Geographical migration and fitness dynamics of Streptococcus pneumoniae. Nature, 631(8020), 386-392. https://doi.org/10.2139/ssrn.4654774
Berube, B. J., & Bubeck Wardenburg, J. (2013). Staphylococcus aureus α-toxin: nearly a century of intrigue. Toxins, 5(6), 1140-1166. https://doi.org/10.3390/toxins5061140
Bleul, L., Francois, P., & Wolz, C. (2022). Two-component systems of S. aureus: signaling and sensing mechanisms. Genes, 13(1), 34. https://doi.org/10.3390/genes13010034
Boisset, S., Geissmann, T., Huntzinger, E., Fechter, P., Bendridi, N., Possedko, M., Chevalier, C., Helfer, A. C., Benito, Y., Jacquier, A., Gaspin, C., Vandenesch, F., & Romby, P. (2007). Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes & Development, 21(11), 1353-1366. https://doi.org/10.1101/gad.423507
Bose, J. L., Wollenberg, M. S., Colton, D. M., Mandel, M. J., Septer, A. N., Dunn, A. K., & Stabb, E. V. (2011). Contribution of rapid evolution of the luxR-luxI intergenic region to the diverse bioluminescence outputs of Vibrio fischeri strains isolated from different environments. Applied and Environmental Microbiology, 77(7), 2445-2457. https://doi.org/10.1128/AEM.02643-10
Brouwer, S., Rivera-Hernandez, T., Curren, B. F., Harbison-Price, N., De Oliveira, D. M. P., Jespersen, M. G., Davies, M. R., & Walker, M. J. (2023). Pathogenesis, epidemiology and control of Group A Streptococcus infection. Nature Reviews Microbiology, 21(7), 431-447. https://doi.org/10.1038/s41579-023-00865-7
Campbell, E. A., Choi, S. Y., & Masure, H. R. (1998). A competence regulon in Streptococcus pneumoniae revealed by genomic analysis. Molecular Microbiology, 27(5), 929-939. https://doi.org/10.1046/j.1365-2958.1998.00737.x
Chang, J. C., Wilkening, R. V., Rahbari, K. M., & Federle, M. J. (2022). Quorum sensing regulation of a major facilitator superfamily transporter affects multiple streptococcal virulence factors. Journal of Bacteriology, 204(9), e00176-22. https://doi.org/10.1128/jb.00176-22
Cheung, G. Y., Joo, H. S., Chatterjee, S. S., & Otto, M. (2014). Phenol-soluble modulins-critical determinants of staphylococcal virulence. FEMS Microbiology Reviews, 38(4), 698-719. https://doi.org/10.1111/1574-6976.12057
Cheung, G. Y. C., Kretschmer, D., Duong, A. C., Yeh, A. J., Ho, T. V., Chen, Y., Joo, H. S., Villaruz, A. E., Roberts, A. W., Lu, Q., Peschel, A., & Otto, M. (2014). Production of an attenuated phenol-soluble modulin variant unique to the MRSA clonal complex 30 increases severity of bloodstream infection. PLoS Pathogens, 10(8), e1004298. https://doi.org/10.1371/journal.ppat.1004298
Cheung, G. Y., Wang, R., Khan, B. A., Sturdevant, D. E., & Otto, M. (2011). Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infection and Immunity, 79(5), 1927-1935. https://doi.org/10.1128/IAI.00046-11
Crossley, K. B., Jefferson, K. K., Archer, G. L., & Fowler Jr, V. G. (Eds.). (2009). Staphylococci in human disease. Wiley-Blackwell. https://doi.org/10.1002/9781444308464
Cvitkovitch, D. G., Li, Y. H., & Ellen, R. P. (2003). Quorum sensing and biofilm formation in Streptococcal infections. The Journal of Clinical Investigation, 112(11), 1626-1632. https://doi.org/10.1172/JCI200320430
Dastgheyb, S. S., Villaruz, A. E., Le, K. Y., Tan, V. Y., Duong, A. C., Chatterjee, S. S., Cheung, A. L., Parvizi, J., & Otto, M. (2015). Role of phenol-soluble modulins in formation of Staphylococcus aureus biofilms in synovial fluid. Infection and Immunity, 83(7), 2966-2975. https://doi.org/10.1128/IAI.00394-15
De Saizieu, A., Gardès, C., Flint, N., Wagner, C., Kamber, M., Mitchell, T. J., Keck, W., Amrein, K. E., & Lange, R. (2000). Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide. Journal of Bacteriology, 182(17), 4696-4703. https://doi.org/10.1128/JB.182.17.4696-4703.2000
Esposito, S., Masetti, M., Calanca, C., Canducci, N., Rasmi, S., Fradusco, A., & Principi, N. (2025). Recent changes in the epidemiology of group A Streptococcus infections: Observations and implications. Microorganisms, 13(8), 1871. https://doi.org/10.3390/microorganisms13081871
Feldstein, S. F., Rahbari, K. M., Leonardo, T. R., Alvernaz, S. A., McIntire, I., Foster, R., & Federle, M. J. (2025). The Streptococcus pyogenes Rgg2/Rgg3 quorum sensing system causes global suppression of macrophage inflammatory programs via an intranuclear mechanism. mBio, 16(11), e00373-25. https://doi.org/10.1128/mbio.00373-25
Fowler, V. G., Jr., Sakoulas, G., McIntyre, L. M., Meka, V. G., Arbeit, R. D., Cabell, C. H., McIntyre, L. F., Boucher, H. W., Corey, G. R., Kramer, P. A., Karchmer, A. W., & Bayer, A. S. (2004). Persistent bacteremia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombin-induced platelet microbicidal protein. The Journal of Infectious Diseases, 190(6), 1140-1149. https://doi.org/10.1086/423145
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(2), 269-275. https://doi.org/10.1128/jb.176.2.269-275.1994
Galante, J., Ho, A. C., Tingey, S., & Charalambous, B. M. (2015). Quorum sensing and biofilms in the pathogen, Streptococcus pneumoniae. Current Pharmaceutical Design, 21(1), 25-30. https://doi.org/10.2174/1381612820666140905113336
Gómez, M. I., Lee, A., Reddy, B., Muir, A., Soong, G., Pitt, A., Cheung, A., & Prince, A. (2004). Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nature Medicine, 10(8), 842-848. https://doi.org/10.1038/nm1079
Jimenez, J. C., & Federle, M. J. (2014). Quorum sensing in group A Streptococcus. Frontiers in Cellular and Infection Microbiology, 4, 127. https://doi.org/10.3389/fcimb.2014.00127
Joo, H. S., Chan, J. L., Cheung, G. Y., & Otto, M. (2010). Subinhibitory concentrations of protein synthesis-inhibiting antibiotics promote increased expression of the agr virulence regulator and production of phenol-soluble modulin cytolysins in community-associated methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 54, 4942-4944. https://doi.org/10.1128/AAC.00064-10
Khan, B. A., Yeh, A. J., Cheung, G. Y., & Otto, M. (2015). Investigational therapies targeting quorum-sensing for the treatment of Staphylococcus aureus infections. Expert Opinion on Investigational Drugs, 24(5), 689-704. https://doi.org/10.1517/13543784.2015.1019062
Klymnyuk, S. I., & Romanyuk, L. B. (2024). Deiaki osoblyvosti mikrobiomu liudyny [Some features of human microbiome]. Infektsiini khvoroby, (4), 33-42. [In Ukrainian]. https://doi.org/10.11603/1681-2727.2024.4.15005
Koenig, R. L., Ray, J. L., Maleki, S. J., Smeltzer, M. S., & Hurlburt, B. K. (2004). Staphylococcus aureus AgrA binding to the RNAIII-agr regulatory region. Journal of Bacteriology, 186, 7549-7555. https://doi.org/10.1128/JB.186.22.7549-7555.2004
Kolar, S. L., Ibarra, J. A., Rivera, F. E., Mootz, J. M., Davenport, J. E., Stevens, S. M., Horswill, A. R., & Shaw, L. N. (2013). Extracellular proteases are key mediators of Staphylococcus aureus virulence via the global modulation of virulence‐determinant stability. MicrobiologyOpen, 2(1), 18-34. https://doi.org/10.1002/mbo3.55
Le, K. Y., & Otto, M. (2015). Quorum-sensing regulation in staphylococci-an overview. Frontiers in Microbiology, 6, 1174. https://doi.org/10.3389/fmicb.2015.01174
Lee, M. S., & Morrison, D. A. (1999). Identification of a new regulator in Streptococcus pneumoniae linking quorum sensing to competence for genetic transformation. Journal of Bacteriology, 181(16), 5004-5016. https://doi.org/10.1128/JB.181.16.5004-5016.1999
Li, M., Villaruz, A. E., Vadyvaloo, V., Sturdevant, D. E., & Otto, M. (2008). AI-2-dependent gene regulation in Staphylococcus epidermidis. BMC Microbiology, 8(1), 4. https://doi.org/10.1186/1471-2180-8-4
Li, Y. H., Lau, P. C., Lee, J. H., Ellen, R. P., & Cvitkovitch, D. G. (2001). Natural genetic transformation of Streptococcus mutans growing in biofilms. Journal of Bacteriology, 183(3), 897-908. https://doi.org/10.1128/JB.183.3.897-908.2001
Li, Y. H., Lau, P. C., Tang, N., Svensäter, G., Ellen, R. P., & Cvitkovitch, D. G. (2002a). Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. Journal of Bacteriology, 184(22), 6333-6342. https://doi.org/10.1128/JB.184.22.6333-6342.2002
Li, Y. H., Tang, N., Aspiras, M. B., Lau, P. C., Lee, J. H., Ellen, R. P., & Cvitkovitch, D. G. (2002b). A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. Journal of Bacteriology, 184(10), 2699-2708. https://doi.org/10.1128/JB.184.10.2699-2708.2002
Liao, Z., & Li, W. (2025). Research progress on quorum sensing in the caries-causing effects of Streptococcus mutans and Candida albicans. Journal of Prevention and Treatment for Stomatological Diseases, 33(4), 328-335.
Liu, Y., & Liu, J. (2022). Group B Streptococcus: virulence factors and pathogenic mechanism. Microorganisms, 10(12), 2483. https://doi.org/10.3390/microorganisms10122483
Lu, Y., Lin, Y., Li, M., & He, J. (2023). Roles of Streptococcus mutans-Candida albicans interaction in early childhood caries: a literature review. Frontiers in Cellular and Infection Microbiology, 13, 1151532. https://doi.org/10.3389/fcimb.2023.1151532
Majchrzykiewicz, J. A., Lubelski, J., Moll, G. N., Kuipers, A., Bijlsma, J. J., Kuipers, O. P., & Rink, R. (2010). Production of a class II two-component lantibiotic of Streptococcus pneumoniae using the class I nisin synthetic machinery and leader sequence. Antimicrobial Agents and Chemotherapy, 54(4), 1498-1505. https://doi.org/10.1128/AAC.00883-09
Maricic, N., Anderson, E. S., Opipari, A. E., Yu, E. A., & Dawid, S. (2016). Characterization of a multipeptide lantibiotic locus in Streptococcus pneumoniae. mBio, 7, e01656-15. https://doi.org/10.1128/mBio.01656-15
Matsumoto, M., Nakagawa, S., Zhang, L., Nakamura, Y., Villaruz, A. E., Otto, M., Wolz, C., Inohara, N., & Núñez, G. (2021). Interaction between Staphylococcus Agr virulence and neutrophils regulates pathogen expansion in the skin. Cell Host & Microbe, 29(6), 930-940. https://doi.org/10.1016/j.chom.2021.03.007
Mendonca, M. L., Szamosi, J. C., Lacroix, A. M., Fontes, M. E., Bowdish, D. M., & Surette, M. G. (2017). The sil locus in Streptococcus anginosus group: Interspecies competition and a hotspot of genetic diversity. Frontiers in Microbiology, 7, 2156. https://doi.org/10.3389/fmicb.2016.02156
Merritt, J., & Qi, F. (2012). The mutacins of Streptococcus mutans: regulation and ecology. Molecular Oral Microbiology, 27(2), 57-69. https://doi.org/10.1111/j.2041-1014.2011.00634.x
Merritt, J., Qi, F., Goodman, S. D., Anderson, M. H., & Shi, W. (2003). Mutation of luxS affects biofilm formation in Streptococcus mutans. Infection and Immunity, 71(4), 1972-1979. https://doi.org/10.1128/IAI.71.4.1972-1979.2003
Mussbacher, M., Derler, M., Basílio, J., & Schmid, J. A. (2023). NF-κB in monocytes and macrophages-an inflammatory master regulator in multitalented immune cells. Frontiers in Immunology, 14, 1134661. https://doi.org/10.3389/fimmu.2023.1134661
Nizet, V., Beall, B., Bast, D. J., Datta, V., Kilburn, L., Low, D. E., & De Azavedo, J. C. (2000). Genetic locus for streptolysin S production by group A streptococcus. Infection and Immunity, 68(7), 4245-4254. https://doi.org/10.1128/IAI.68.7.4245-4254.2000
Ong, C. J. N., Elesho, O. E., Bramwell, B. B., Cabuhat, K. S. P., Bacalzo, G. D., Nuevo, J. J. M., & Fortaleza, J. A. G. (2025). Staphylococcus aureus: Antimicrobial resistance, quorum sensing, and antibiofilm approaches. European Journal of Microbiology and Immunology, 15(4), 195-209. https://doi.org/10.1556/1886.2025.00050
Opdyke, J. A., Scott, J. R., & Moran Jr, C. P. (2003). Expression of the secondary sigma factor σX in Streptococcus pyogenes is restricted at two levels. Journal of Bacteriology, 185(15), 4291-4297. https://doi.org/10.1128/JB.185.15.4291-4297.2003
Park, J., Jagasia, R., Kaufmann, G. F., Mathison, J. C., Ruiz, D. I., Moss, J. A., Meijler, M. M., Ulevitch, R. J., & Janda, K. D. (2007). Infection control by antibody disruption of bacterial quorum sensing signaling. Chemistry & Biology, 14(10), 1119-1127. https://doi.org/10.1016/j.chembiol.2007.08.013
Paulander, W., Nissen Varming, A., Baek, K. T., Haaber, J., Frees, D., & Ingmer, H. (2013). Antibiotic-mediated selection of quorum-sensing-negative Staphylococcus aureus. mBio, 3, e00459-12. https://doi.org/10.1128/mBio.00459-12
Pauli, N. T., Kim, H. K., Falugi, F., Huang, M., Dulac, J., Henry Dunand, C., Zheng, N., & Wilson, P. C. (2014). Staphylococcus aureus infection induces protein A-mediated immune evasion in humans. Journal of Experimental Medicine, 211(12), 2331-2339. https://doi.org/10.1084/jem.20141404
Periasamy, S., Joo, H. S., Duong, A. C., Bach, T. H. L., Tan, V. Y., Chatterjee, S. S., Cheung, G. Y. C., & Otto, M. (2012). How Staphylococcus aureus biofilms develop their characteristic structure. Proceedings of the National Academy of Sciences, 109(4), 1281-1286. https://doi.org/10.1073/pnas.1115006109
Peterson, S., Cline, R. T., Tettelin, H., Sharov, V., & Morrison, D. A. (2000). Gene expression analysis of the Streptococcus pneumoniae competence regulons by use of DNA microarrays. Journal of Bacteriology, 182(21), 6192-6202. https://doi.org/10.1128/JB.182.21.6192-6202.2000
Pinkston, K. L., Gao, P., Diaz-Garcia, D., Sillanpää, J., Nallapareddy, S. R., Murray, B. E., & Harvey, B. R. (2011). The Fsr quorum-sensing system of Enterococcus faecalis modulates surface display of the collagen-binding MSCRAMM Ace through regulation of gelE. Journal of Bacteriology, 193(17), 4317-4325. https://doi.org/10.1128/JB.05026-11
Powers, M. E., Kim, H. K., Wang, Y., & Bubeck Wardenburg, J. (2012). ADAM10 mediates vascular injury induced by Staphylococcus aureus α-hemolysin. Journal of Infectious Diseases, 206(3), 352-356. https://doi.org/10.1093/infdis/jis192
Queck, S. Y., Jameson-Lee, M., Villaruz, A. E., Bach, T. H. L., Khan, B. A., Sturdevant, D. E., Ricklefs, S. M., Kuroda, M., & Otto, M. (2008). RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Molecular Cell, 32(1), 150-158. https://doi.org/10.1016/j.molcel.2008.08.005
Rinaldi, A. J., Lund, P. E., Blanco, M. R., & Walter, N. G. (2016). The Shine-Dalgarno sequence of riboswitch-regulated single mRNAs shows ligand-dependent accessibility bursts. Nature Communications, 7(1), 8976. https://doi.org/10.1038/ncomms9976
Rudkin, J. K., Laabei, M., Edwards, A. M., Joo, H. S., Otto, M., Lennon, K. L., O'Keeffe, K. M., Waterfield, N. R., Massey, R. C., & O'Gara, J. P. (2014). Oxacillin alters the toxin expression profile of community-associated methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 58, 1100-1107. https://doi.org/10.1128/AAC.01618-13
Rued, B. E., Covington, B. C., Bushin, L. B., Szewczyk, G., Laczkovich, I., Seyedsayamdost, M. R., & Federle, M. J. (2021). Quorum sensing in Streptococcus mutans regulates production of tryglysin, a novel ras-ripp antimicrobial compound. mBio, 12(2), e02688-20. https://doi.org/10.1128/mBio.02688-20
Said-Salim, B., Dunman, P. M., McAleese, F. M., Macapagal, D., Murphy, E., McNamara, P. J., Arvidson, S., Tjaden, B., Projan, S. J., & Kreiswirth, B. N. (2003). Global regulation of Staphylococcus aureus genes by Rot. Journal of Bacteriology, 185(2), 610-619. https://doi.org/10.1128/JB.185.2.610-619.2003
Sangiorgio, G., Calvo, M., Migliorisi, G., Campanile, F., & Stefani, S. (2024). The impact of Enterococcus spp. in the immunocompromised host: a comprehensive review. Pathogens, 13(5), 409. https://doi.org/10.3390/pathogens13050409
Stroeher, U. H., Paton, A. W., Ogunniyi, A. D., & Paton, J. C. (2003). Mutation of luxS of Streptococcus pneumoniae affects virulence in a mouse model. Infection and Immunity, 71(6), 3206-3212. https://doi.org/10.1128/IAI.71.6.3206-3212.2003
Sully, E. K., Malachowa, N., Elmore, B. O., Alexander, S. M., Femling, J. K., Gray, B. M., DeLeo, F. R., Otto, M., Cheung, A. L., Edwards, B. S., Sklar, L. A., Horswill, A. R., & Gresham, H. D. (2014). Selective chemical inhibition of agr quorum sensing in Staphylococcus aureus promotes host defense with minimal impact on resistance. PLoS Pathogens, 10(6), e1004174. https://doi.org/10.1371/journal.ppat.1004174
Szafrański, S. P., Deng, Z. L., Tomasch, J., Jarek, M., Bhuju, S., Rohde, M., Sztajer, H., & Wagner-Döbler, I. (2017). Quorum sensing of Streptococcus mutans is activated by Aggregatibacter actinomycetemcomitans and by the periodontal microbiome. BMC Genomics, 18(1), 238. https://doi.org/10.1186/s12864-017-3618-5
Traber, K. E., Lee, E., Benson, S., Corrigan, R., Cantera, M., Shopsin, B., & Novick, R. P. (2008). agr function in clinical Staphylococcus aureus isolates. Microbiology, 154(8), 2265-2274. https://doi.org/10.1099/mic.0.2007/011874-0
Vuong, C., Gerke, C., Somerville, G. A., Fischer, E. R., & Otto, M. (2003). Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. The Journal of Infectious Diseases, 188(5), 706-718. https://doi.org/10.1086/377239
Vuong, C., Kocianova, S., Yao, Y., Carmody, A. B., & Otto, M. (2004). Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo. The Journal of Infectious Diseases, 190(8), 1498-1505. https://doi.org/10.1086/424487
Vuong, C., Saenz, H. L., Götz, F., & Otto, M. (2000). Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. The Journal of Infectious Diseases, 182(6), 1688-1693. https://doi.org/10.1086/317606
Wang, R., Khan, B. A., Cheung, G. Y. C., Bach, T. H. L., Jameson-Lee, M., Kong, K. F., Queck, S. Y., & Otto, M. (2011). Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. Journal of Clinical Investigation, 121(1), 238-248. https://doi.org/10.1172/JCI42520
Wang, W., Singh, P. K., Bojer, M. S., Savijoki, K., Yli-Kauhaluoma, J., Ingmer, H., & Fulaz, S. (2025). Inhibition of agr Quorum Sensing in Staphylococci by Novel Thiazole-Indole Hybrid Compounds. bioRxiv, 10. https://doi.org/10.1101/2025.10.15.682726
Waters, C. M., & Bassler, B. L. (2005). Quorum sensing: cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology, 21(1), 319-346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
Wen, J. D., Kuo, S. T., & Chou, H. H. D. (2021). The diversity of Shine-Dalgarno sequences sheds light on the evolution of translation initiation. RNA Biology, 18(11), 1489-1500. https://doi.org/10.1080/15476286.2020.1861406
Wenderska, I. B., Lukenda, N., Cordova, M., Magarvey, N., Cvitkovitch, D. G., & Senadheera, D. B. (2012). A novel function for the competence inducing peptide, XIP, as a cell death effector of Streptococcus mutans. FEMS Microbiology Letters, 336(2), 104-112. https://doi.org/10.1111/j.1574-6968.2012.02660.x
Wilke, G. A., & Wardenburg, J. B. (2010). Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus α-hemolysin-mediated cellular injury. Proceedings of the National Academy of Sciences, 107(30), 13473-13478. https://doi.org/10.1073/pnas.1001815107
Wright III, J. S., Jin, R., & Novick, R. P. (2005). Transient interference with staphylococcal quorum sensing blocks abscess formation. Proceedings of the National Academy of Sciences, 102(5), 1691-1696. https://doi.org/10.1073/pnas.0407661102
Xavier, K. B., & Bassler, B. L. (2003). LuxS quorum sensing: more than just a numbers game. Current Opinion in Microbiology, 6(2), 191-197. https://doi.org/10.1016/S1369-5274(03)00028-6
Xu, L., Li, H., Vuong, C., Vadyvaloo, V., Wang, J., Yao, Y., Otto, M., & Gao, Q. (2006). Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infection and Immunity, 74(1), 488-496. https://doi.org/10.1128/IAI.74.1.488-496.2006
Yu, D., Zhao, L., Xue, T., & Sun, B. (2012). Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner. BMC Microbiology, 12(1), 288. https://doi.org/10.1186/1471-2180-12-288
Zhang, L., & Ji, G. (2004). Identification of a staphylococcal AgrB segment (s) responsible for group-specific processing of AgrD by gene swapping. Journal of Bacteriology, 186(20), 6706-6713. https://doi.org/10.1128/JB.186.20.6706-6713.2004
Zhao, L., Xue, T., Shang, F., Sun, H., & Sun, B. (2010). Staphylococcus aureus AI-2 quorum sensing associates with the KdpDE two-component system to regulate capsular polysaccharide synthesis and virulence. Infection and Immunity, 78(8), 3506-3515. https://doi.org/10.1128/IAI.00131-10
Downloads
Published
Issue
Section
License
Copyright (c) 2026 Mikrobiolohichnyi Zhurnal
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
