Inara E Laryushina

DOI: 10.33284/2658-3135-103-4-160

UDC 576.8.078

Acknowledgements:

Research was carried out according the plan of research scientific works on 2019-2021 yy. FSBSI FRC BST RAS (No 0526-2019-0002)

The main mechanisms of "quorum sense" and their implementation in

       multimicrobial community (review)

Inara E Laryushina

Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences (Orenburg, Russia)

Summary. The study of the molecular mechanisms of quorum sensing today, undoubtedly, remains an urgent and demanded task. At the same time, the features of complex communication systems of the multi-microbial community are increasingly appearing in the focus of attention of leading research teams. Bacterial cells do not exist in isolation, and therefore relationships between bacterial systems, as well as with the host organism, are ubiquitous. The successful functioning of populations of microorganisms in the natural environment is largely due to a complex system of intercellular interaction. Communication of this kind is called Quorum Sensing (QS), which is a system for coordinating gene expression and depends on the density of the bacterial population, and its implementation occurs using small signaling molecules. Currently, a large number of microorganisms have been identified that have a sense of quorum. In addition, recent studies indicate that this process is also a mechanism for interspecies and interregnum interactions, including with higher eukaryotes. The review presents the molecular mechanisms underlying the biosynthesis of autoinducers, detection of intercellular signals, information processing, and post-transcriptional control of quorum sensing, as well as some ways of QS implementation in the multimicrobial community.

Key words: microorganisms, quorum sensing, multimicrobial community, interspecies interaction.

References

  1. Abaturov AE, Kruchko TA. Drugs inhibiting the quorum-sensing of bacteria staphylococcus aureus. Child’s Health. 2019;14(3):189-197. doi: 10.22141/2224-0551.14.3.2019.168803
  2. Zaitseva YuV. Molecular genetic features of Quorum Sensing systems of gram-negative bacteria (on the Serratia model) and study of their role in the regulation of cellular processes [dissertation] Moscow; 2012:157 p.
  3. Koukleva LM, Eroshenko GA. Intercellular communication quorum sensing in pathogenic bacteria of the genus Yersinia. Problems of Particularly Dangerous infections. 2009;4(102):54-59. doi:https://doi.org/10.21055/0370-1069-2009-4(102)-54-59
  4. Mayansky AN, Chebotar IV. Strategy of control for bacterial biofilm processes. Journal Infectology. 2012;4(3):5-15.
  5. Danilov VS, Zavilgelsky GB, Zarubina AP, Mazhul MM. The role of luxCDE-genes in bioluminescence of  bacteria. Moscow University Bulletin. Series 16. Biology. 2008;2:11-15.
  6. Khaitovich AB, Mureiko EA. Quorum sensing of microorganisms as a factor of pathogenicity. Tavrichesky Medical and Biological Bulletin. 2018;21(1):206-212.
  7. Ball AS, Chaparian RR, van Kessel JC. Quorum sensing gene regulation by LuxR/HapR master regulators in vibrios. Journal of Bacteriology. 2017;199(19):e00105-17. doi: 10.1128/JB.00105-17
  8. Barriuso J, Hogan DA, Keshavarz T, Martínez MJ. Role of quorum sensing and chemical communication in fungal biotechnology and pathogenesis. FEMS Microbiology Reviews. 2018;42(5):627-638. doi:10.1093/femsre/fuy022
  9. Baruch M, Belotserkovsky I, Hertzog BB, Ravins M, Dov E, McIver KS, Hanski E et al. An extracellular bacterial pathogen modulates host metabolism to regulate its own sensing and proliferation. Cell. 2014;156(1-2):97-108. doi: 10.1016/j.cell.2013.12.007
  10. Camps J et al. Paraoxonases as potential antibiofilm agents: their relationship with quorum-sensing signals in  gram-negative  bacteria.  Antimicrob  Agents   Chemother. 2011;55(4):1325-1331. doi: 10.1128/AAC.01502-10
  11. Chen X, Zhang L, Zhang M, Liu H, Lu P, Lin K. Quorum sensing inhibitors: a patent review (2014-2018). Expert  Opinion  on Therapeutic Patents. 2018;28(12):849-865. doi: 10.1080/13543776.2018.1541174
  12. Chang JC, LaSarre B, Jimenez JC, Aggarwal C, Federle MJ. Two group A streptococcal peptide pheromones act through opposing Rgg regulators to control biofilm development. PLoS Pathog. 2011;7(8):e1002190. doi: 10.1371/journal.ppat.1002190
  13. Chugani S, Greenberg EP. An evolving perspective on the Pseudomonas aeruginosa orphan quorum sensing regulator QscR. Front Cell Infect Microbiol. 2014;4:152. doi: 10.3389/fcimb.2014.00152
  14. Cook LC, LaSarre B, Federle MJ. Interspecies communication among commensal and pathogenic streptococci. Mbio. 2013;4(4):e00382-13. doi: 10.1128/mBio.00382-13
  15. Daddaoua A, Fillet S, Fernández M, Udaondo Z, Krell T, Ramos JL. Genes for carbon metabolism and the ToxA virulence factor in Pseudomonas aeruginosa are regulated through molecular interactions of PtxR and PtxS. PLoS One. 2012;7(7):e39390. doi:https://doi.org/10.1371/journal.pone.0039390
  16. Date SV, Modrusan Z, Lawrence M, Morisaki JH, Toy K, Shah IM, etal. Global gene expression of methicillin-resistant Staphylococcus aureus USA300 during human and mouse infection. J Infect Dis. 2014;209(10):1542-1550. doi: 10.1093/infdis/jit668
  17. Feng L, Rutherford ST, Papenfort K, Bagert JD, van Kessel JC, Tirrell DA, Wingreen NS, Bassler BL. A Qrr non-coding RNA deploys four different regulatory mechanisms to optimize quorum-sensing dynamics. Cell. 2015;160(1-2):228-240. doi: 10.1016/j.cell.2014.11.051
  18. Fleuchot B, Gitton C, Guillot A, Vidic J, Nicolas P, Besset C, Fontaine L, Hols P, Leblond-Bourget N, Monnet V, Gardan R. Rgg proteins associated with internalized small hydrophobic peptides: a new quorum-sensing mechanism in streptococci. Mol Microbiol. 2011;80(4):1102-1119. doi:10.1111/j.1365-2958.2011.07633.x
  19. Gauthier GM. Dimorphism in fungal pathogens of mammals, plants, and insects. PLoS Pathog. 2015;11(2):e1004608. doi: 10.1371/journal.ppat.1004608
  20. Hudaiberdiev S, et al. Census of solo LuxR genes in prokaryotic genomes. Front Cell Infect Microbiol. 2015;5:20. doi: 10.3389/fcimb.2015.00020
  21. Jimenez JC, Federle MJ. Quorum sensing in group A Streptococcus. Front Cell Infect Microbiol. 2014;4:127. doi: 10.3389/fcimb.2014.00127
  22. Kendall MM, Sperandio V. Cell-to-cell signaling in E. coli and Salmonella. EcoSal Plus. 2014;6(1). doi: 10.1128/ecosalplus.ESP-0002-2013
  23. Khan BA, Yeh AJ, Cheung GY, Otto M. Investigational therapies targeting quorum-sensing for the treatment of Staphylococcus aureus infections. Expert Opin Investig Drugs. 2015;24(5):689-704. doi: 10.1517/13543784.2015.1019062
  24. Kolar SL, Ibarra JA, Rivera FE, Mootz JM, Davenport JE, Stevens SM, et al. Extracellular proteases are key mediators of Staphylococcus aureus virulence via the global modulation of virulence-determinant stability. Microbiology Open. 2013;2(1):18-34. doi:10.1002/mbo3.55
  25. Le KY, Otto M. Quorum-sensing regulation in staphylococci – an overview. Frontiers in Microbiology. 2015;6:1174. doi: 10.3389/fmicb.2015.01174
  26. Lee J, Zhang L. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein & Cell. 2015;6(1):26-41. doi: 10.1007/s13238-014-0100-x
  27. Lupp C, Urbanowski M, Greenberg EP, Ruby EG. The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol Microbiol. 2003;50(1):319-331. doi: 10.1046/j.1365-2958.2003.t01-1-03585.x
  28. Mattmann ME, Blackwell HE. Small molecules that modulate quorum sensing and control virulence in Pseudomonas aeruginosa. J Org Chem. 2010;75(20):6737-6746. doi: https://doi.org/10.1021/jo101237e
  29. Mony BM, MacGregor P, Ivens A et al. Genome-wide dissection of the quorum sensing signalling pathway in Trypanosoma brucei. Nature. 2014;505:681-685. doi: 10.1038/nature12864
  30. Murray EJ, Crowley RC, Truman A, et al. Targeting Staphylococcus aureus quorum sensing with nonpeptidic small molecule inhibitors. J Med Chem. 2014;57(6):2813-2819. doi:10.1021/jm500215s
  31. Ng WL, Bassler BL. Bacterial quorum-sensing network architectures. Annual review of genetics. 2009;43:197-222. doi: 10.1146/annurev-genet-102108-134304
  32. Padder SA, Prasad R, Shah AH. Quorum sensing: A less known mode of communication among fungi. Microbiological research. 2018;210:51-58. doi:10.1016/j.micres.2018.03.007
  33. Papenfort K, Bassler BL. Quorum sensing signal–response systems in Gram-negative bacteria. Nat Rev Microbiol. 2016;14:576-88. doi: 10.1038/nrmicro.2016.89
  34. Polke M, Jacobsen ID. Quorum sensing by farnesol revisited. Current Genetics. 2017;63(5):791-797. doi: https://doi.org/10.1007/s00294-017-0683-x
  35. Prescott RD, Decho AW. Flexibility and adaptability of quorum sensing in nature. Trends in Microbiology. 2020;28(6):436-444. doi: https://doi.org/10.1016/j.tim.2019.12.004
  36. Rémy B, Mion S, Plener L, Elias M, Chabrière E, Daudé D. Interference in bacterial quorum sensing: a biopharmaceutical perspective. Frontiers in pharmacology. 2018;9:203. doi: https://doi.org/10.3389/fphar.2018.00203
  37. Rojas F, Silvester E, Young J, Milne R, Tettey M, Houston DR, Smith TK, et al. Oligopeptide signaling through TbGPR89 drives trypanosome quorum sensing. Cell. 2019;176(1-2):306-317. doi: 10.1016/j.cell.2018.10.041
  38. Ruby EG. Lessons from a cooperative, bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light  organ symbiosis. Annu Rev Microbiol. 1996;50:591-624. doi: 10.1146/annurev.micro.50.1.591
  39. Schuster M, Sexton DJ, Diggle SP, Greenberg EP. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol. 2013;67:43-63. doi: 10.1146/annurev-micro-092412-155635
  40. Schaefer AL, Greenberg EP, Oliver CM, Oda Y, Huang JJ, et al. A new class of homoserine lactone quorum-sensing signals. Nature. 2008;454:595-599. doi: 10.1038/nature07088
  41. Steindler L, Venturi V. Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol Lett. 2007; 266(1):1-9. doi: https://doi.org/10.1111/j.1574-6968.2006.00501.x
  42. Sun J, Daniel R, Wagner-Döbler I, Zeng AP. Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evolutionary Biology. 2004;4(1):36. doi: 10.1186/1471-2148-4-36
  43. Svenningsen SL. Small RNA‐based regulation of bacterial quorum sensing and biofilm formation. In: Storz G, Papenfort K (eds), Regulating with RNA in Bacteria and Archaea. Washington, DC: ASM Press; 2019; 283-304. doi: 10.1128/microbiolspec.RWR-0017-2018
  44. Subramoni S et al. A bioinformatic survey of distribution, conservation, and probable functions of LuxR  solo  regulators  in  bacteria. Front Cell Infect Microbiol. 2015;5:16. doi: https://doi.org/10.3389/fcimb.2015.00016
  45. Sudbery PE. Growth of Candida albicans hyphae. Nat Rev Microbiol. 2011;9:737-748.
  46. Tarnita CE, Washburne A, Martinez-Garcia R, et al. Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds. Proc Natl Acad Sci USA 2015;112(9):2776-2781). doi: 10.1073/pnas.1424242112
  47. Tu KC, Bassler BL. Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev. 2007;21:221-233. doi:10.1101/gad.1502407
  48. Venturi V, Subramoni S, Sabag-Daigle A, Ahmer BM. Methods to study solo/orphan quorum-sensing receptors. In: Leoni L, Rampioni G (eds), Quorum Sensing. Methods in Molecular Biology. NY: Humana Press. 2018;1673:145-159. doi: https://doi.org/10.1007/978-1-4939-7309-5_12
  49. Vogt SL, Pena-Diaz J, Finlay BB. Chemical communication in the gut: Effects of microbiota-generated metabolites on gastrointestinal bacterial pathogens. Anaerobe. 2015;34:106-115. doi: 10.1016/j.anaerobe.2015.05.002
  50. Westwater C, Balish E, Schofield DA. Candida albicans-conditioned medium protects yeast cells from oxidative stress: a possible link between quorum sensing and oxidative stress resistance. Eukaryot Cell. 2005;4(10):1654-1661. doi: 10.1128/EC.4.10.1654-1661.2005
  51. Whiteley M, Diggle SP, Greenberg EP. Bacterial quorum sensing: the progress and promise of an emerging research area. Nature. 2017;551(7680):313-320. doi: 10.1038/nature24624
  52. Xue T, Zhao L, Sun B. LuxS/AI-2system is involved in antibiotic Susceptibility and autolysis in Staphylococcus aureus NCTC8325. Int.J. Antimicrob.Agents. 2013;41(1):85-89. doi: 10.1016/j.ijantimicag.2012.08.016
  53. Yu D, Zhao L, Xue T, Sun B. Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in anica R-dependent manner. BMC Microbiol. 2012;12:288.doi:10.1186/1471-2180-12-288
  54. Zimmermann H, Subota I, Batram C, Kramer S, Janzen CJ, Jones NG, Engstler M. A quorum sensing-independent path to stumpy development in Trypanosoma brucei. PLoS pathogens. 2017;13(4):e1006324. doi: https://doi.org/10.1371/journal.ppat.1006324

Laryushina Inara Eskenderovna, Cand. Sci. (Med.), Researcher, Laboratory of Selection and Genetic Research in Livestock, Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences, 460000, Orenburg, Russia, 9 Yanvarya St., 29, tel.: +79033658342, e-mail: inhip@mail.ru

Received: 30 November 2020; Accepted: 14 December 2020; Published: 31 December 2020

Download