Bacteria-to-bacteria communication, Signaling Molecules: AHLs, AIPs and AI-2, I can't talk now matey, gone to pathogenesis!

Year 2023, Volume: 10 Issue: 4, 590 - 604, 01.12.2023

Nurdan Filik , Fethi Filik

Abstract

How do these primitive tiny organisms' hierarchy operate? The answer is simple: by communicating. Yes, bacteria talk, and it’s called: Quorum Sensing System (QS). QS is a phenomenon where bacteria tinychat and arrange their moves via the accumulation of signaling molecules. The cells respond to this stimulus when the cut-off value concentration of molecules is achieved. This phenomenon is widespreadly visible in the bacteria world. Bacteria never move solo and would need to gather up in critical mass because of secrete efficient toxins to be lethal. N-Acyl Homoserine Lactones (AHLs): Intercellular signaling molecules used by Gram-negative bacteria (Gram-) to monitor their critical mass density in QS controlling of critic gene expression. AHL signals are synthesized by LuxI proteins. AHLs are vital interbacterial signaling molecules used by bacteria to check their dependent bacteria density. Auto-inducing peptides (AIPs): signaling molecules involved in intercellular communication in Gram-positive bacteria (Gram+). Peptides are exported by dedicated systems, post-translationally modified and eventually sensed by other bacteria cells via membrane-located receptors that are part of a two-component system. AI-2 (Autoinducer-2): signaling molecule used by interspecies bacteria communication. This molecule chemically identified furanosylborate diester synthesized by LuxS proteins. Also, it's a universal signal because it carries out interspecies communication. The aim of this review is to summarize the AHL, AIPs, AI-2 bacterial signal molecules, QS systems target genes, effective in the procaryotic world, and the micro-social lifestyle of bacteria.

Keywords

Signal Molecules: AHLs, AIPs AI-2, Quorum Sensing System, Bacterially Speaking, Bacteria-to-bacteria Communication, Interbacterial Communication

References

• Andersen, J.B., Heydorn, A., Hentzer, M., Eberl, L.E.O., Geisenberger, O., Christensen, B.B., ... & Givskov, M. (2001). gfp-based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Applied and Environmental Microbiology, 67(2), 575-585.
• Bainton, N.J., Bycroft, B.W., Chhabra, S.R., Stead, P., Gledhill, L., Hill, P.J., … & Williams, P. (1992). A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. Gene, 116(1), 87-91.
• Bao, J., Guo, D., Jin, L., Li, T., & Shi, H. (2022). Accurate Identification of Diverse N-acyl Homoserine Lactones in Marine Vibrio fluvialis by UHPLC-MS/MS. Current Microbiology, 79(6), 1-11.
• Bassler, B.L. (1999). How bacteria talk to each other: regulation of gene expression by quorum sensing. Current Opinion in Microbiology, 2(6), 582-587.
• Brackman, G., Coenye, T. (2015). Quorum sensing inhibitors as anti-biofilm agents. Current Pharmaceutical Design, 21(1), 5-11.
• Bruhn, J.B., Dalsgaard, I., Nielsen, K.F., Buchholtz, C., Larsen, J.L., & Gram, L. (2005). Quorum sensing signal molecules (acylated homoserine lactones) in gram-negative fish pathogenic bacteria. Diseases of aquatic organisms, 65(1), 43-52.
• Burr, T., Barnard, A.M., Corbett, M.J., Pemberton, C.L., Simpson, N.J., & Salmond, G.P. (2006). Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Molecular microbiology, 59(1), 113-125.
• Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B.L., & Hughson, F.M. (2002). Structural identification of a bacterial quorum-sensing signal containing boron. Nature, 415(6871), 545-549.
• Deepa, N., Chauhan, S., Kumari, P., Rai, A.K., Tandon, S., & Singh, A. (2022). Linalool reduces the virulence of Pseudomonas syringae pv. tomato DC 3000 by modulating the PsyI/PsyR quorum-sensing system. Microbial Pathogenesis, 105884.
• Eberl, L., Winson, M.K., Sternberg, C., Stewart, G.S., Christiansen, G., Chhabra, S.R., ... & Givskov, M. (1996). Involvement of N‐acyl‐l‐homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Molecular microbiology, 20(1), 127-136.
• Frommberger, M., Schmitt-Kopplin, P., Ping, G., Frisch, H., Schmid, M., Zhang, Y., ... & Kettrup, A. (2004). A simple and robust set-up for on-column sample preconcentration–nano-liquid chromatography–electrospray ionization mass spectrometry for the analysis of N-acylhomoserine lactones. Analytical and bioanalytical chemistry, 378(4), 1014-1020.
• Fuqua, C., Winans, S.C., & Greenberg, E.P. (1996). Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annual review of microbiology, 50, 727-752.
• Geske, G.D., O’Neill, J.C., & Blackwell, H.E. (2008). Expanding dialogues: from natural autoinducers to non-natural analogues that modulate quorum sensing in Gram-negative bacteria. Chemical Society Reviews, 37(7), 1432-1447.
• Huang, S., Zhang, H., Ng, T.C.A., Xu, B., Shi, X., & Ng, H.Y. (2020). Analysis of N-Acy-L-homoserine lactones (AHLs) in wastewater treatment systems using SPE-LLE with LC-MS/MS. Water Research, 177, 115756.
• Huang, Q., Chen, J., Zhu, J., Hao, X., Dao, G., Chen, W., ... & Huang, Q. (2021). Divergent bacterial transformation exerted by soil minerals. Science of The Total Environment, 784, 147173.
• Jin, L., Zhang, X., Shi, H., Wang, W., Qiao, Z., Yang, W., & Du, W. (2020). Identification of a novel N-acyl Homoserine lactone synthase, AhyI, in Aeromonas hydrophila and structural basis for its substrate specificity. Journal of Agricultural and Food Chemistry, 68(8), 2516-2527.
• Kim, S.R., & Yeon, K.M. (2018). Quorum sensing as language of chemical signals. In Comprehensive Analytical Chemistry, 81, 57-94. Elsevier.
• Konai, M.M., Dhanda, G., & Haldar, J. (2018). Talking through chemical languages: quorum sensing and bacterial communication. In Quorum sensing and its biotechnological applications, 17-42. Springer, Singapore.
• Kumari, A., Pasini, P., Deo, S.K., Flomenhoft, D., Shashidhar, H., & Daunert, S. (2006). Biosensing systems for the detection of bacterial quorum signaling molecules. Analytical Chemistry, 78(22), 7603-7609.
• Laj, N., Elayadeth-Meethal, M., Huxley, V.A.J., Hussain, R.R., Kuruniyan, M.S., & Naseef, P.P. (2022). Quorum-sensing molecules: Sampling, identification and characterization of N-acyl-homoserine lactone in Vibrio sp. Saudi Journal of Biological Sciences, 29(4), 2733-2737. https://doi.org/10.1016/j.sjbs.2021.12.062
• LaSarre, B., & Federle, M.J. (2013). Exploiting quorum sensing to confuse bacterial pathogens. Microbiology and Molecular Biology Reviews, 77(1), 73-111.
• Lerat, E., & Moran, N.A. (2004). The evolutionary history of quorum-sensing systems in bacteria. Molecular Biology and Evolution, 21(5), 903-913.
• Lewis, H.A., Furlong, E.B., Laubert, B., Eroshkina, G.A., Batiyenko, Y., Adams, J.M., ... & Buchanan, S.G. (2001). A structural genomics approach to the study of quorum sensing: crystal structures of three LuxS orthologs. Structure, 9(6), 527-537.
• Liu, X., Liu, Q., Sun, S., Sun, H., Wang, Y., Shen, X., & Zhang, L. (2022). Exploring AI-2-mediated interspecies communications within rumen microbial communities. Microbiome, 10(1), 1-16.
• Malone, C.L., Boles, B.R., & Horswill, A.R. (2007). Biosynthesis of Staphylococcus aureus autoinducing peptides by using the synechocystis DnaB mini-intein. Applied and Environmental Microbiology, 73(19), 6036-6044.
• Marin, S.D.L., Xu, Y., Meijler, M.M., & Janda, K.D. (2007). Antibody catalyzed hydrolysis of a quorum sensing signal found in Gram-negative bacteria. Bioorganic & Medicinal Chemistry Letters, 17(6), 1549-1552.
• Mayville, P., Ji, G., Beavis, R., Yang, H., Goger, M., Novick, R.P., & Muir, T.W. (1999) Structureactivity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc Natl Acad Sci USA 96, 1218-1223. https://doi.org/10.1046/j.1365-2958.2001.02539.x
• McClean, K.H., Winson, M.K., Fish, L., Taylor, A., Chhabra, S.R., Camara, M., ... & Williams, P. (1997). Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology, 143(12), 3703-3711.
• Milton, D.L., Hardman, A., Camara, M., Chhabra, S.R., Bycroft, B.W., Stewart, G.S., & Williams, P. (1997). Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone. J Bacteriol, 179, 3004–3012. https://doi.org/10.1128/jb.179.9.3004-3012.1997
• Miller, M.B., & Bassler, B.L. (2001). Quorum sensing in bacteria. Annual Review of Microbiology, 55(1), 165-199.
• Miller, S.T., Xavier, K.B., Campagna, S.R., Taga, M.E., Semmelhack, M.F., Bassler, B.L., & Hughson, F.M. (2004). Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorumsensing signal AI-2. Molecular Cell, 15, 677–687. https://doi.org/10.1016/j.molcel.2004.07.020
• Rajput, A., Kaur, K., & Kumar, M. (2016). SigMol: repertoire of quorum sensing signaling molecules in prokaryotes. Nucleic Acids Research, 44(D1), D634-D639.
• Parveen, N., & Cornell, K.A. (2011). Methylthioadenosine/S‐adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism. Molecular Microbiology, 79(1), 7-20.
• Pereira, H., Azevedo, F., Rego, A., Sousa, M.J., Chaves, S.R., & Côrte-Real, M. (2013) The protective role of yeast cathepsin D in acetic acid-induced apoptosis depends on ANT (Aac2p) but not on the voltage-dependent channel (Por1p). FEBS Lett, 587, 200–205. https://doi.org/10.1016/j. febslet.2012.11.025
• Pütz, E., Gazanis, A., Keltsch, N.G., Jegel, O., Pfitzner, F., Heermann, R., ... & Tremel, W. (2022). Communication Breakdown: Into the Molecular Mechanism of Biofilm Inhibition by CeO2 Nanocrystal Enzyme Mimics and How It Can Be Exploited. ACS Nano, 16(10), 16091-16108.
• Qiao, Z., Li, J., & Qin, S. (2022). Bioactive Compounds for Quorum Sensing Signal-Response Systems in Marine Phycosphere. Journal of Marine Science and Engineering, 10(5), 699.
• Rosario, M.E., Diou-Cass, Q., Harvey, E., Whalen, K., & Rowley, D.C. (2022). Production of signaling molecules by the marine bacterium Pseudoalteromonas galatheae and implications for antagonistic interactions with the bloom forming coccolithophore Emiliania huxleyi. Chemical Investigation of Metabolites Produced by Marine Pseudoalteromonas spp., 42.
• Rutherford, S.T., Bassler, B.L. (2012). Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor perspectives in medicine, 2(11), a012427.
• Sahreen, S., Mukhtar, H., Imre, K., Morar, A., Herman, V., & Sharif, S. (2022). Exploring the function of quorum sensing regulated biofilms in biological wastewater treatment: A review. International Journal of Molecular Sciences, 23(17), 9751.
• Schaefer, A.L., Harwood, C.S., & Greenberg, E.P. (2018). “Hot stuff”: The many uses of a radiolabel assay in detecting acyl-homoserine lactone quorum-sensing signals. In Quorum Sensing, 35-47. Humana Press.
• Soni, K., Jesudhasan, P., Cepeda, M., Williams, B., Hume, M., Russell, W.K., ... & Pillai, S.D., (2007). Proteomic analysis to identify the role of LuxS/AI-2 mediated protein expression in Escherichia coli O157: H7. Foodborne Pathogens and Disease, 4(4), 463-471.
• Sundar, K., Prabu, R., & Jayalakshmi, G. (2022). Quorum Sensing Inhibition Based Drugs to Conquer Antimicrobial Resistance. The Global Antimicrobial Resistance Epidemic: Innovative Approaches and Cutting-Edge Solutions, 199.
• Swift, S., Winson, M.K., Chan, P.F., Bainton, N.J., Birdsall, M., Reeves, P.J., ... & Stewart, G.S.A.B. (1993). A novel strategy for the isolation of luxl homologues: evidence for the widespread distribution of a LuxR: Luxl superfamily in enteric bacteria. Molecular Microbiology, 10(3), 511-520.
• Swift, S., Karlyshev, A.V., Fish, L., Durant, E.L., Winson, M.K., Chhabra, S.R., ... & Stewart, G. (1997). Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. Journal of Bacteriology, 179(17), 5271-5281.
• Thirunavukkarasu, R., Pandi, P., Pushparaj, S., Subramanian, K., & Arokiarajan, M. S. (2023). Quorum sensing relationship analysis of microbial symbionts. Microbial Symbionts, 831.
• Wang, J., Quan, C., Wang, X., Zhao, P., & Fan, S. (2011). Extraction, purification and identification of bacterial signal molecules based on N‐acyl homoserine lactones. Microbial Biotechnology, 4(4), 479-490.
• MDowell, P., Affas, Z., Reynolds, C., Holden, M.T., Wood, S.J., Saint, S., Cockayne, A., Hill, P.J., Dodd, C.E., Bycroft, B.W., Chan, W.C., & Williams, P. (2001). Structure, activity and evolution of the group I thioM. M. Konai et al. lactone peptide quorum-sensing system of Staphylococcus aureus. Mol Microbiol, 41, 503–512.
• Winsberg, M. (2022). Speaking in Thumbs: A Psychiatrist Decodes Your Relationship Texts So You Don't Have to. Doubleday.
• Winzer, K., Hardie, K.R., & Williams, P. (2002). Bacterial cell-to-cell communication: sorry, can't talk now—gone to lunch!. Current Opinion in Microbiology, 5(2), 216-222.
• Wynendaele, E., Bronselaer, A., Nielandt, J., D’Hondt, M., Stalmans, S., Bracke, N., ... & De Spiegeleer, B. (2013). Quorumpeps database: chemical space, microbial origin and functionality of quorum sensing peptides. Nucleic Acids Research, 41(D1), D655-D659.
• Wynendaele, E., Gevaert, B., Stalmans, S., Verbeke, F., & De Spiegeleer, B. (2015). Exploring the chemical space of quorum sensing peptides. Peptide Science, 104(5), 544-551.
• von Rad, U., Klein, I., Dobrev, P.I., Kottova, J., Zazimalova, E., Fekete, A., ... & Durner, J. (2008). Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta, 229(1), 73-85.
• Yang, T., Tal-Gan, Y., Paharik, A.E., Horswill, A.R., & Blackwell, H.E. (2016). Structure-function analyses of a Staphylococcus epidermidis autoinducing peptide reveals motifs critical for AgrC-type receptor modulation. ACS Chem Biol, 11, 1982–1991. https://doi.org/10.1021/acschembio.6b00120
• Zavilgelsky, G.B., & Manukhov, I.V. (2001). Quorum sensing, or how bacteria “talk” to each other. Molecular Biology, 35(2), 224-232.
• Zhang, Z., & Pierson III, L.S. (2001). A second quorum-sensing system regulates cell surface properties but not phenazine antibiotic production in Pseudomonas aureofaciens. Applied and Environmental Microbiology, 67(9), 4305-4315.