420
Views
2
CrossRef citations to date
0
Altmetric
Review Articles

Quorum sensing in biofilms: a key mechanism to target in ecotoxicological studies

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 786-804 | Received 21 Mar 2022, Accepted 26 Oct 2022, Published online: 05 Nov 2022

References

  • Ahator SD, Zhang L. 2019. Small Is mighty—chemical communication systems in Pseudomonas aeruginosa. Annu Rev Microbiol. 73(1):559–578.
  • Ali SG, Ansari MA, Jamal QMS, Khan HM, Jalal M, Ahmad H, Mahdi AA. 2017. Antiquorum sensing activity of silver nanoparticles in P. aeruginosa: an in silico study. Silico Pharmacol. 5(1):1–7.
  • Al-Shabib NA, Husain FM, Hassan I, Khan MS, Ahmed F, Qais FA, Oves M, Rahman M, Khan RA, Khan A, et al. 2018. Biofabrication of zinc oxide nanoparticle from Ochradenus baccatus leaves: broad-spectrum antibiofilm activity, protein binding studies, and in vivo toxicity and stress studies. J Nanomater. 2018:1–14.
  • Angenent LT, Karim K, Al-Dahhan MH, Wrenn BA, Domíguez-Espinosa R. 2004. Production of bioenergy and biochemicals from industrial and agricultural wastewater. Trends Biotechnol. 22(9):477–485.
  • Azam F, Fenchel T, Field JG, Gray J, Meyer-Reil L, Thingstad F. 1983. The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser. 10:257–263.
  • Babić F, Venturi V, Maravić-Vlahoviček G. 2010. Tobramycin at subinhibitory concentration inhibits the RhlI/R quorum sensing system in a Pseudomonas aeruginosa environmental isolate. BMC Infect Dis. 10(1):148.
  • Battin TJ, Besemer K, Bengtsson MM, Romani AM, Packmann AI. 2016. The ecology and biogeochemistry of stream biofilms. Nat Rev Microbiol. 14(4):251–263.
  • Biswa P, Doble M. 2013. Production of acylated homoserine lactone by gram-positive bacteria isolated from marine water. FEMS Microbiol Lett. 343(1):34–41.
  • Blanchet E, Prado S, Stien D, Oliveira da Silva J, Ferandin Y, Batailler N, Intertaglia L, Escargueil A, Lami R. 2017. Quorum sensing and quorum quenching in the Mediterranean seagrass Posidonia oceanica microbiota. Front Mar Sci. 4:218.
  • Boyd RS. 2010. Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol. 36(1):46–58.
  • Bulich A, Greene M, Isenberg D. 1981. Reliability of the bacterial luminescence assay for determination of the toxicity of pure compounds and complex effluents. In Branson D, Dickson K, editors. Aquatic toxicology and hazard assessment. West Conshohocken, PA: ASTM International; p. 338–347.
  • Bulich A, Isenberg D. 1981. Use of the luminescent bacterial system for the rapid assessment of aquatic toxicity. ISA Trans. 20(1):29–33.
  • Buzea C, Pacheco II, Robbie K. 2007. Nanomaterials and nanoparticles: sources and toxicity. Biointerphases. 2(4):MR17–MR71.
  • Bzdrenga J, Daudé D, Remy B, Jacquet P, Plener L, Elias M, Chabriere E. 2017. Biotechnological applications of quorum quenching enzymes. Chem Biol Interact. 267:104–115.
  • Cai S, Shen Y, Zou Y, Sun P, Wei W, Zhao J, Zhang C. 2018. Engineering highly sensitive whole-cell mercury biosensors based on positive feedback loops from quorum-sensing systems. Analyst. 143(3):630–634.
  • Case RJ, Labbate M, Kjelleberg S. 2008. AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. Isme J. 2(4):345–349.
  • Chabert N, Bonnefoy V, Achouak W. 2018. Quorum sensing improves current output with Acidithiobacillus ferrooxidans. Microb Biotechnol. 11(1):136–140.
  • Chang I-S, Le Clech P, Jefferson B, Judd S. 2002. Membrane fouling in membrane bioreactors for wastewater treatment. J Environ Eng. 128(11):1018–1029.
  • Chen A, Huang Y. 2020. Acyl homoserine lactone based quorum sensing affects phenanthrene removal by Novosphingobium pentaromativorans US6-1 through altering cell surface properties. Int Biodeterior Biodegrad. 147:104841.
  • Chong G, Kimyon O, Rice SA, Kjelleberg S, Manefield M. 2012. The presence and role of bacterial quorum sensing in activated sludge. Microb Biotechnol. 5(5):621–633.
  • Chugani S, Greenberg EP. 2010. LuxR homolog-independent gene regulation by acyl-homoserine lactones in Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 107(23):10673–10678.
  • Colvin VL. 2003. The potential environmental impact of engineered nanomaterials. Nat Biotechnol. 21(10):1166–1170.
  • Conway BA, Greenberg E. 2002. Quorum-sensing signals and quorum-sensing genes in Burkholderia vietnamiensis. J Bacteriol. 184(4):1187–1191.
  • Dang H, Lovell CR. 2016. Microbial surface colonization and biofilm development in marine environments. Microbiol Mol Biol Rev. 80(1):91–138.
  • De Kreuk M, Kishida N, Van Loosdrecht M. 2007. Aerobic granular sludge–state of the art. Water Sci Technol. 55(8-9):75–81.
  • De Windt W, Boon N, Siciliano SD, Verstraete W. 2003. Cell density related H2 consumption in relation to anoxic Fe (0) corrosion and precipitation of corrosion products by Shewanella oneidensis MR‐1. Environ Microbiol. 5(11):1192–1202.
  • Decho AW, Visscher PT, Ferry J, Kawaguchi T, He L, Przekop KM, Norman RS, Reid RP. 2009. Autoinducers extracted from microbial mats reveal a surprising diversity of N‐acylhomoserine lactones (AHLs) and abundance changes that may relate to diel pH. Environ Microbiol. 11(2):409–420.
  • Defoirdt T, Crab R, Wood TK, Sorgeloos P, Verstraete W, Bossier P. 2006. Quorum sensing-disrupting brominated furanones protect the gnotobiotic brine shrimp Artemia franciscana from pathogenic Vibrio harveyi, Vibrio campbellii, and Vibrio parahaemolyticus isolates. Appl Environ Microbiol. 72(9):6419–6423.
  • Doberva M, Sanchez-Ferandin S, Toulza E, Lebaron P, Lami R. 2015. Diversity of quorum sensing autoinducer synthases in the Global Ocean Sampling metagenomic database. Aquat Microb Ecol. 74(2):107–119.
  • Dobretsov S, Teplitski M, Paul V. 2009. Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling. 25(5):413–427.
  • D’Souza S. 2001. Microbial biosensors. Biosens Bioelectron. 16(6):337–353.
  • Dusane DH, Zinjarde SS, Venugopalan VP, Mclean RJ, Weber MM, Rahman PK. 2010. Quorum sensing: implications on rhamnolipid biosurfactant production. Biotechnol Genet Eng Rev. 27(1):159–184.
  • Eberhard A. 1972. Inhibition and activation of bacterial luciferase synthesis. J Bacteriol. 109(3):1101–1105.
  • Eberhard A, Burlingame AL, Eberhard C, Kenyon G, Nealson KH, Oppenheimer N. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry. 20(9):2444–2449.
  • El-Gohary N, Shaaban M. 2014. Antimicrobial and antiquorum-sensing studies. Part 2: synthesis, antimicrobial, antiquorum-sensing and cytotoxic activities of new series of fused [1, 3, 4] thiadiazole and [1, 3] benzothiazole derivatives. Med Chem Res. 23(1):287–299.
  • Elias M, Tawfik DS. 2012. Divergence and convergence in enzyme evolution: parallel evolution of paraoxonases from quorum-quenching lactonases. J Biol Chem. 287(1):11–20.
  • Engebrecht J, Nealson K, Silverman M. 1983. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell. 32(3):773–781.
  • Faust K, Raes J. 2012. Microbial interactions: from networks to models. Nat Rev Microbiol. 10(8):538–550.
  • Feng H, Ding Y, Wang M, Zhou G, Zheng X, He H, Zhang X, Shen D, Shentu J. 2014. Where are signal molecules likely to be located in anaerobic granular sludge? Water Res. 50:1–9.
  • Flemming HC, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol. 8(9):623–633.
  • Flemming HC, Wuertz S. 2019. Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol. 17(4):247–260.
  • Foght J, Westlake D. 1988. Degradation of polycyclic aromatic hydrocarbons and aromatic heterocycles by a Pseudomonas species. Can J Microbiol. 34(10):1135–1141.
  • Fuqua WC, Winans SC, Greenberg EP. 1994. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol. 176(2):269–275.
  • Gagné F. 2017. Toxicity and disruption of quorum sensing in Aliivibrio fisheri by environmental chemicals: impacts of selected contaminants and microplastics. J Xenobiot. 7(1):7101.
  • Galindo-Miranda JM, Guízar-González C, Becerril-Bravo EJ, Moeller-Chávez G, León-Becerril E, Vallejo-Rodríguez R. 2019. Occurrence of emerging contaminants in environmental surface waters and their analytical methodology – a review. Water Supply. 19(7):1871–1884.
  • Gao B, Chi L, Tu P, Bian X, Thomas J, Ru H, Lu K. 2018. The organophosphate malathion disturbs gut microbiome development and the quorum-sensing system. Toxicol Lett. 283:52–57.
  • Gao C, Zeng YH, Li CY, Li L, Cai ZH, Zhou J. 2022. Bisphenol A biodegradation by Sphingonomas sp. YK5 is regulated by acyl-homoserine lactone signaling molecules. Sci Total Environ. 802:149898.
  • García-Contreras R, Nunez-Lopez L, Jasso-Chávez R, Kwan BW, Belmont JA, Rangel-Vega A, Maeda T, Wood TK. 2015. Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating. ISME J. 9(1):115–125.
  • Ghangrekar M, Chatterjee P. 2018. Water pollutants classification and its effects on environment. Carbon Nanotubes Clean Water. Berlin, Germany: Springer; p. 11–26.
  • Ghosal D, Ghosh S, Dutta TK, Ahn Y. 2016. Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol. 7:1369.
  • Gómez-Gómez B, Arregui L, Serrano S, Santos A, Pérez-Corona T, Madrid Y. 2019. Unravelling mechanisms of bacterial quorum sensing disruption by metal-based nanoparticles. Sci Total Environ. 696:133869.
  • Grandclement C, Tannieres M, Morera S, Dessaux Y, Faure D. 2016. Quorum quenching: role in nature and applied developments. FEMS Microbiol Rev. 40(1):86–116.
  • Greenberg E, Hastings J, Ulitzur S. 1979. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol. 120(2):87–91.
  • Guasch H, Artigas J, Bonet B, Bonnineau C, Canals O, Corcoll N, Foulquier A, Lopez-Doval J, Kim Tiam S, Morin S, et al. 2016. The use of biofilms to assess the effects of chemicals on freshwater ecosystems. Aquatic biofilms: ecology, water quality and wastewater treatment. Cambridge (MA): Academic Press; p. 125–144.
  • Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2(2):95–108.
  • Haque S, Yadav DK, Bisht SC, Yadav N, Singh V, Dubey KK, Jawed A, Wahid M, Dar SA. 2019. Quorum sensing pathways in Gram-positive and-negative bacteria: potential of their interruption in abating drug resistance. J Chemother. 31(4):161–187.
  • Haritash A, Kaushik C. 2009. Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater. 169(1-3):1–15.
  • Hartmann A, Schikora A. 2012. Quorum sensing of bacteria and trans-kingdom interactions of N-acyl homoserine lactones with eukaryotes. J Chem Ecol. 38(6):704–713.
  • Hayat S, Muzammil S, Aslam B, Siddique MH, Saqalein M, Nisar, MA,  Shabana. 2019. Quorum quenching: role of nanoparticles as signal jammers in Gram-negative bacteria. Future Microbiol. 14(1):61–72.
  • Hayek M, Baraquet C, Lami R, Blache Y, Molmeret M. 2020. The marine bacterium Shewanella woodyi produces C8-HSL to regulate bioluminescence. Microb Ecol. 79(4):865–881.
  • He J, Zhang X, Qian Y, Wang Q, Bai Y. 2022. An engineered quorum-sensing-based whole-cell biosensor for active degradation of organophosphates. Biosens Bioelectron. 206:114085.
  • Head IM, Jones DM, Röling WF. 2006. Marine microorganisms make a meal of oil. Nat Rev Microbiol. 4(3):173–182.
  • Hmelo LR. 2017. Quorum sensing in marine microbial environments. Ann Rev Mar Sci. 9:257–281.
  • Hobman JL, Crossman LC. 2015. Bacterial antimicrobial metal ion resistance. J Med Microbiol. 64(Pt 5):471–497.
  • Hsu CY, Chen BK, Hu RH, Chen BS. 2016. Systematic design of a quorum sensing-based biosensor for enhanced detection of metal ion in Escherichia coli. IEEE Trans Biomed Circuits Syst. 10(3):593–601.
  • Huang J, Shi Y, Zeng G, Gu Y, Chen G, Shi L, Hu Y, Tang B, Zhou J. 2016. Acyl-homoserine lactone-based quorum sensing and quorum quenching hold promise to determine the performance of biological wastewater treatments: an overview. Chemosphere. 157:137–151.
  • Huang S, Bergonzi C, Schwab M, Elias M, Hicks RE. 2019. Evaluation of biological and enzymatic quorum quencher coating additives to reduce biocorrosion of steel. PLoS One. 14(5):e0217059.
  • Huang Y, Zeng Y, Yu Z, Zhang J, Feng H, Lin X. 2013. In silico and experimental methods revealed highly diverse bacteria with quorum sensing and aromatics biodegradation systems–a potential broad application on bioremediation. Bioresour Technol. 148:311–316.
  • Iranzo M, Sainz-Pardo I, Boluda R, Sanchez J, Mormeneo S. 2001. The use of microorganisms in environmental remediation. Ann Microbiol. 51(2):135–144.
  • Jacobson GA. 2007. Corrosion at Prudhoe Bay: a lesson on the line. Mater Perform. 46(8):26–34.
  • Ji Y, Yu H, Cao R, Xu X, Zhu L. 2022. Promoting the granulation process of aerobic sludge via a sustainable strategy of effluent reflux in view of AHLs-mediated quorum sensing. J Environ Manage. 303:114091.
  • Jia R, Unsal T, Xu D, Lekbach Y, Gu T. 2019. Microbiologically influenced corrosion and current mitigation strategies: a state of the art review. Int Biodeterior Biodegrad. 137:42–58.
  • Joelsson A, Kan B, Zhu J. 2007. Quorum sensing enhances the stress response in Vibrio cholerae. Appl Environ Microbiol. 73(11):3742–3746.
  • Joint I, Tait K, Callow ME, Callow JA, Milton D, Williams P, Camara M. 2002. Cell-to-cell communication across the prokaryote-eukaryote boundary. Science. 298(5596):1207.
  • Jothinathan DAN, Raman P. 2018. Applications of quorum sensing in microbial fuel cell. Quorum sensing and its biotechnological applications. Berlin, Germany: Springer; p. 167–177.
  • Jurado-Martín I, Sainz-Mejías M, McClean S. 2021. Pseudomonas aeruginosa: an audacious pathogen with an adaptable arsenal of virulence factors. Int J Mol Sci. 22(6):3128.
  • Kang Y, Park W. 2010. Contribution of quorum-sensing system to hexadecane degradation and biofilm formation in Acinetobacter sp. strain DR1. J Appl Microbiol. 109(5):1650–1659.[20629796.
  • Kang YS, Jung J, Jeon CO, Park W. 2011. Acinetobacter oleivorans sp. nov. is capable of adhering to and growing on diesel-oil. J Microbiol. 49(1):29–34.
  • Kashyap DR, Botero LM, Franck WL, Hassett DJ, McDermott TR. 2006. Complex regulation of arsenite oxidation in Agrobacterium tumefaciens. J Bacteriol. 188(3):1081–1088.
  • Kirschner CM, Brennan AB. 2012. Bio-inspired antifouling strategies. Annu Rev Mater Res. 42(1):211–229.
  • Klaschka U. 2008. The infochemical effect—a new chapter in ecotoxicology. Environ Sci Pollut Res Int. 15(6):452–462.
  • Koch GH, Brongers MP, Thompson NG, Virmani YP, Payer JH. 2001. Corrosion cost and preventive strategies in the United States. Washington (DC): Federal Highway Administration. Report FHWA-RD-01-XXX.
  • Kuizu S, Ruiyu W, Hui Z, Wei W, Tianwei H. 2022. Mechanism and regulation of filamentous algal-bacterial symbiosis based on microbiological quorum sensing. Water Environ Res. 94(3):e10697.
  • Kumari S, Mangwani N, Das S. 2016. Synergistic effect of quorum sensing genes in biofilm development and PAHs degradation by a marine bacterium. Bioengineered. 7(3):205–211.
  • Lade H, Paul D, Kweon JH. 2014. Isolation and molecular characterization of biofouling bacteria and profiling of quorum sensing signal molecules from membrane bioreactor activated sludge. Int J Mol Sci. 15(2):2255–2273.
  • Lami R. 2019. Chapter 3 - Quorum sensing in marine biofilms and environments. In: Tommonaro G, editor. Cambridge (MA): Academic Press; p. 55–96.
  • Lami R, Jones LC, Cottrell MT, Lafferty BJ, Ginder-Vogel M, Sparks DL, Kirchman DL. 2013. Arsenite modifies structure of soil microbial communities and arsenite oxidization potential. FEMS Microbiol Ecol. 84(2):270–279.
  • Lead JR, Batley GE, Alvarez PJJ, Croteau M-N, Handy RD, McLaughlin MJ, Judy JD, Schirmer K. 2018. Nanomaterials in the environment: behavior, fate, bioavailability, and effects-An updated review: nanomaterials in the environment. Environ Toxicol Chem. 37(8):2029–2063.
  • Learman DR, Yi H, Brown SD, Martin SL, Geesey GG, Stevens AM, Hochella MF. 2009. Involvement of Shewanella oneidensis MR-1 LuxS in biofilm development and sulfur metabolism. Appl Environ Microbiol. 75(5):1301–1307.
  • Lee J, Wu J, Deng Y, Wang J, Wang C, Wang J, Chang C, Dong Y, Williams P, Zhang LH. 2013. A cell-cell communication signal integrates quorum sensing and stress response. Nat Chem Biol. 9(5):339–343.
  • Lee J, Zhang L. 2015. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell. 6(1):26–41.
  • Lei Y, Chen W, Mulchandani A. 2006. Microbial biosensors. Anal Chim Acta. 568(1–2):200–210.
  • Li X, Liu Y, Wang Y, Lin Z, Wang D, Sun H. 2021. Resistance risk induced by quorum sensing inhibitors and their combined use with antibiotics: mechanism and its relationship with toxicity. Chemosphere. 265:129153.
  • Liang X, Yu X, Pan X, Wu J, Duan Y, Wang J, Zhou M. 2018. A thiadiazole reduces the virulence of Xanthomonas oryzae pv. oryzae by inhibiting the histidine utilization pathway and quorum sensing. Mol Plant Pathol. 19(1):116–128.
  • Lillicrap A, Macken A, Wennberg AC, Grung M, Rundberget JT, Fredriksen L, Scheie AA, Benneche T, d‘Auriac MA. 2016. Environmental fate and effects of novel quorum sensing inhibitors that can control biofilm formation. Chemosphere. 164:52–58.
  • Liu X, Sun S, Ma B, Zhang C, Wan C, Lee D-J. 2016. Understanding of aerobic granulation enhanced by starvation in the perspective of quorum sensing. Appl Microbiol Biotechnol. 100(8):3747–3755.
  • Liu Y, Guo J, Lian J, Chen Z, Li Y, Xing Y, Wang T. 2018. Effects of extracellular polymeric substances (EPS) and N-acyl-L-homoserine lactones (AHLs) on the activity of anammox biomass. Int Biodeterior Biodegrad. 129:141–147.
  • Living with Resistance Project. 2018. Antibiotic and pesticide susceptibility and the Anthropocene operating space. Nat Sustain. 1(11):632–641.
  • Logan BE. 2009. Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol. 7(5):375–381.
  • Madsen EL. 2005. Identifying microorganisms responsible for ecologically significant biogeochemical processes. Nat Rev Microbiol. 3(5):439–446.
  • Maier RM, Gentry TJ. 2015. Microorganisms and organic pollutants. Environmental microbiology. 3rd ed. Amsterdam, Netherlands: Elsevier; p. 377–413.
  • Markus V, Share O, Shagan M, Halpern B, Bar T, Kramarsky-Winter E, Teralı K, Özer N, Marks RS, Kushmaro A, et al. 2021. Inhibitory effects of artificial sweeteners on bacterial quorum sensing. Int J Mol Sci. 22(18):9863.
  • Maynard AD. 2011. Don’t define nanomaterials. Nature. 475(7354):31.
  • McGivney E, Jones KE, Weber B, Valentine AM, VanBriesen JM, Gregory KB. 2018. Quorum sensing signals form complexes with Ag + and Cu 2+ cations. ACS Chem Biol. 13(4):894–899.
  • McLean RJ, Whiteley M, Stickler DJ, Fuqua WC. 1997. Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol Lett. 154(2):259–263.
  • Milaković M, Vestergaard G, González-Plaza JJ, Petrić I, Šimatović A, Senta I, Kublik S, Schloter M, Smalla K, Udiković-Kolić N. 2019. Pollution from azithromycin-manufacturing promotes macrolide-resistance gene propagation and induces spatial and seasonal bacterial community shifts in receiving river sediments. Environ Int. 123:501–511.
  • Miller MB, Bassler BL. 2001. Quorum sensing in bacteria. Annu Rev Microbiol. 55(1):165–199.
  • Mohanty A, Tan CH, Cao B. 2016. Impacts of nanomaterials on bacterial quorum sensing: differential effects on different signals. Environ Sci Nano. 3(2):351–356.
  • Molnár M, Fenyvesi É, Berkl Z, Németh I, Fekete-Kertész I, Márton R, Vaszita E, Varga E, Ujj D, Szente L. 2021. Cyclodextrin-mediated quorum quenching in the Aliivibrio fischeri bioluminescence model system – Modulation of bacterial communication. Int J Pharm. 594:120150.
  • Montgomery K, Charlesworth JC, LeBard R, Visscher PT, Burns BP. 2013. Quorum sensing in extreme environments. Life (Basel). 3(1):131–148.
  • Monzon O, Yang Y, Li Q, Alvarez PJ. 2016. Quorum sensing autoinducers enhance biofilm formation and power production in a hypersaline microbial fuel cell. Biochem Eng J. 109:222–227.
  • Morgan-Sagastume F, Boon N, Dobbelaere S, Defoirdt T, Verstraete W. 2005. Production of acylated homoserine lactones by Aeromonas and Pseudomonas strains isolated from municipal activated sludge. Can J Microbiol. 51(11):924–933.
  • Mukherjee S, Bassler BL. 2019. Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol. 17(6):371–382.
  • Muras A, López-Pérez M, Mayer C, Parga A, Amaro-Blanco J, Otero A. 2018. High prevalence of quorum-sensing and quorum-quenching activity among cultivable bacteria and metagenomic sequences in the Mediterranean sea. Genes. 9(2):100.
  • Nadell CD, Xavier JB, Levin SA, Foster KR. 2008. The evolution of quorum sensing in bacterial biofilms. PLoS Biol. 6(1):e14.
  • Naga NG, El-Badan DE, Rateb HS, Ghanem KM, Shaaban MI. 2021. Quorum sensing inhibiting activity of cefoperazone and its metallic derivatives on Pseudomonas aeruginosa. Front Cell Infect Microbiol. 11:716789.[34660340.
  • Naidu R, Espana VAA, Liu Y, Jit J. 2016. Emerging contaminants in the environment: risk-based analysis for better management. Chemosphere. 154:350–357.
  • Nealson KH, Platt T, Hastings JW. 1970. Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol. 104(1):313–322.
  • O’Grady EP, Viteri DF, Malott RJ, Sokol PA. 2009. Reciprocal regulation by the CepIR and CciIR quorum sensing systems in Burkholderia cenocepacia. BMC Genomics. 10(1):441.
  • Oh HS, Kim SR, Cheong WS, Lee CH, Lee JK. 2013. Biofouling inhibition in MBR by Rhodococcus sp. BH4 isolated from real MBR plant. Appl Microbiol Biotechnol. 97(23):10223–10231.
  • Oh HS, Lee CH. 2018. Origin and evolution of quorum quenching technology for biofouling control in MBRs for wastewater treatment. J Membr Sci. 554:331–345.
  • Oh HS, Yeon KM, Yang CS, Kim SR, Lee CH, Park SY, Han JY, Lee JK. 2012. Control of membrane biofouling in MBR for wastewater treatment by quorum quenching bacteria encapsulated in microporous membrane. Environ Sci Technol. 46(9):4877–4884.
  • Otawa K, Lee SH, Yamazoe A, Onuki M, Satoh H, Mino T. 2007. Abundance, diversity, and dynamics of viruses on microorganisms in activated sludge processes. Microb Ecol. 53(1):143–152.
  • Özkaya Ö, Xavier KB, Dionisio F, Balbontín R. 2017. Maintenance of microbial cooperation mediated by public goods in single- and multiple-trait scenarios. J Bacteriol. 199(22):JB.00297-17.
  • Paggi RA, Martone CB, Fuqua C, De Castro RE. 2003. Detection of quorum sensing signals in the haloalkaliphilic archaeon Natronococcus occultus. FEMS Microbiol Lett. 221(1):49–52.
  • Papenfort K, Bassler BL. 2016. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol. 14(9):576–588.
  • Pearson JP, Pesci EC, Iglewski BH. 1997. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol. 179(18):5756–5767.
  • Perry LL, Bright NG, Carroll J, Richard J, Scott MC, Allen MS, Applegate BM. 2005. Molecular characterization of autoinduction of bioluminescence in the Microtox® indicator strain Vibrio fischeri ATCC 49387. Can J Microbiol. 51(7):549–557.
  • Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH. 1999. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 96(20):11229–11234.
  • Piscitelli S, Danziger L, Rodvold K. 1992. Clarithromycin and azithromycin: new macrolide antibiotics. Clin Pharm. 11(2):137–152.
  • Qureshi AA, Bulich AA, Isenberg DL. 2018. Microtox® toxicity test systems—where they stand today. Microscale testing in aquatic toxicology: advances, techniques, and practice. Boca Raton (FL): CRC Press; p. 185–199.
  • Rai R, Ranjan M, Pradhan BB, Chatterjee S. 2012. Atypical regulation of virulence-associated functions by a diffusible signal factor in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact. 25(6):789–801.
  • Raushel FM. 2002. Bacterial detoxification of organophosphate nerve agents. Curr Opin Microbiol. 5(3):288–295.
  • Ravindran D, Ramanathan S, Arunachalam K, Jeyaraj GP, Shunmugiah KP, Arumugam VR. 2018. Phytosynthesized silver nanoparticles as antiquorum sensing and antibiofilm agent against the nosocomial pathogen Serratia marcescens: an in vitro study. J Appl Microbiol. 124(6):1425–1440.
  • Reiss D, Rihm B, Thöni C, Faller M. 2004. Mapping stock at risk and release of zinc and copper in Switzerland—dose response functions for runoff rates derived from corrosion rate data. Water Air Soil Pollut. 159(1):101–113.
  • Ren T, Yu H, Li X. 2010. The quorum-sensing effect of aerobic granules on bacterial adhesion, biofilm formation, and sludge granulation. Appl Microbiol Biotechnol. 88(3):789–797.
  • Riaz K, Elmerich C, Moreira D, Raffoux A, Dessaux Y, Faure D. 2008. A metagenomic analysis of soil bacteria extends the diversity of quorum-quenching lactonases. Environ Microbiol. 10(3):560–570.
  • Ribeiro F, O’Brien JW, Galloway T, Thomas KV. 2019. Accumulation and fate of nano- and micro-plastics and associated contaminants in organisms. TrAC Trends Anal Chem. 111:139–147.
  • Richard H, Carpenter EJ, Komada T, Palmer PT, Rochman CM. 2019. Biofilm facilitates metal accumulation onto microplastics in estuarine waters. Sci Total Environ. 683:600–608.
  • Roane TM, Pepper IL, Gentry TJ. 2015. Microorganisms and metal pollutants. Environmental microbiology. 3rd ed. Amsterdam, Netherlands: Elsevier; p. 415–439.
  • Romani M, Warscheid T, Nicole L, Marcon L, Di Martino P, Suzuki MT, Lebaron P, Lami R. 2022. Current and future chemical treatments to fight biodeterioration of outdoor building materials and associated biofilms: moving away from ecotoxic and towards efficient, sustainable solutions. Sci Total Environ. 802:149846.
  • Romero M, Avendano-Herrera R, Magarinos B, Camara M, Otero A. 2010. Acylhomoserine lactone production and degradation by the fish pathogen Tenacibaculum maritimum, a member of the Cytophaga-Flavobacterium-Bacteroides (CFB) group. FEMS Microbiol Lett. 304(2):131–139.
  • Schorer M, Eisele M. 1997. Accumulation of inorganic and organic pollutants by biofilms in the aquatic environment. Water Air Soil Pollut. 99(1–4):651–659.
  • Seibert CM, Raushel FM. 2005. Structural and catalytic diversity within the amidohydrolase superfamily. Biochemistry. 44(17):6383–6391.
  • Shah S, Gaikwad S, Nagar S, Kulshrestha S, Vaidya V, Nawani N, Pawar S. 2019. Biofilm inhibition and anti-quorum sensing activity of phytosynthesized silver nanoparticles against the nosocomial pathogen Pseudomonas aeruginosa. Biofouling. 35(1):34–49.
  • Sharif DI, Gallon J, Smith CJ, Dudley E. 2008. Quorum sensing in Cyanobacteria: n -octanoyl-homoserine lactone release and response, by the epilithic colonial cyanobacterium Gloeothece PCC6909. ISME J. 2(12):1171–1182.
  • Sheng H, Harir M, Boughner LA, Jiang X, Schmitt-Kopplin P, Schroll R, Wang F. 2017. N-acyl-homoserine lactone dynamics during biofilm formation of a 1,2,4-trichlorobenzene mineralizing community on clay. Sci Total Environ. 605–606:1031–1038.
  • Shen Z, Xu D, Li L, Wang J, Shi X. 2019. Ecological and health risks of heavy metal on farmland soils of mining areas around Tongling City, Anhui, China. Environ Sci Pollut Res Int. 26(15):15698–15709.
  • Singh BR, Singh BN, Singh A, Khan W, Naqvi AH, Singh HB. 2015. Mycofabricated biosilver nanoparticles interrupt Pseudomonas aeruginosa quorum sensing systems. Sci Rep. 5(1):13719–13714.
  • Singh R. 2014. Microorganism as a tool of bioremediation technology for cleaning environment: a review. Proc Int Acad Ecol Environ Sci. 4(1):1.
  • Sivadon P, Barnier C, Urios L, Grimaud R. 2019. Biofilm formation as a microbial strategy to assimilate particulate substrates. Environ Microbiol Rep. 11:749–764.
  • Skindersoe ME, Alhede M, Phipps R, Yang L, Jensen PO, Rasmussen TB, Bjarnsholt T, Tolker-Nielsen T, Høiby N, Givskov M. 2008. Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 52(10):3648–3663.
  • Snow DD, Cassada DA, Bartelt-Hunt SL, Li X, D’Alessio M, Zhang Y, Zhang Y, Sallach JB. 2016. Detection, occurrence and fate of emerging contaminants in agricultural environments. Water Environ Res. 88(10):913–929.
  • Stephenson K, Yamaguchi Y, Hoch JA. 2000. The mechanism of action of inhibitors of bacterial two-component signal transduction systems. J Biol Chem. 275(49):38900–38904.
  • Strom SL. 2008. Microbial ecology of ocean biogeochemistry: a community perspective. Science. 320(5879):1043–1045.
  • Sun GX, Zhou WQ, Zhong JJ. 2006. Organotin decomposition by pyochelin, secreted by Pseudomonas aeruginosa even in an iron-sufficient environment. Appl Environ Microbiol. 72(9):6411–6413.
  • Sun H, Pan Y, Gu Y, Lin Z. 2018. Mechanistic explanation of time-dependent cross-phenomenon based on quorum sensing: A case study of the mixture of sulfonamide and quorum sensing inhibitor to bioluminescence of Aliivibrio fischeri. Sci Total Environ. 630:11–19.
  • Swartzman A, Kapoor S, Graham AF, Meighen EA. 1990. A new Vibrio fischeri lux gene precedes a bidirectional termination site for the lux operon. J Bacteriol. 172(12):6797–6802.
  • Tang X, Guo Y, Wu S, Chen L, Tao H, Liu S. 2018. Metabolomics uncovers the regulatory pathway of acyl-homoserine lactones based quorum sensing in anammox consortia. Environ Sci Technol. 52(4):2206–2216.
  • Tang X, Liu S, Zhang Z, Zhuang G. 2015. Identification of the release and effects of AHLs in anammox culture for bacteria communication. Chem Eng J. 273:184–191.
  • Tateda K, Comte R, Pechere J-C, Köhler T, Yamaguchi K, Van Delden C. 2001. Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 45(6):1930–1933.
  • Thaden JT, Lory S, Gardner TS. 2010. Quorum-sensing regulation of a copper toxicity system in Pseudomonas aeruginosa. J Bacteriol. 192(10):2557–2568.
  • Thornhill SG, Kumar M, Vega LM, McLean RJ. 2017. Cadmium ion inhibition of quorum signalling in Chromobacterium violaceum. Microbiology (Reading). 163(10):1429–1435.
  • Urvoy M, Labry C, L’Helguen S, Lami R. 2022. Quorum sensing regulates bacterial processes that play a major role in marine biogeochemical cycles. Front Mar Sci. 9:834337.
  • Valle A, Bailey MJ, Whiteley AS, Manefield M. 2004. N-acyl-L-homoserine lactones (AHLs) affect microbial community composition and function in activated sludge. Environ Microbiol. 6(4):424–433.
  • Van de Graaf AA, Mulder A, de Bruijn P, Jetten M, Robertson LA, Kuenen JG. 1995. Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol. 61(4):1246–1251.
  • Vega LM, Mathieu J, Yang Y, Pyle BH, McLean RJ, Alvarez PJ. 2014. Nickel and cadmium ions inhibit quorum sensing and biofilm formation without affecting viability in Burkholderia multivorans. Int Biodeterior Biodegrad. 91:82–87.
  • Venturi V. 2006. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev. 30(2):274–291.
  • Walker CH, Sibly R, Hopkin SP, Peakall DB. 2012. Principles of ecotoxicology. 3rd ed. Boca Raton (FL): CRC Press.
  • Wang C, Zhang H, Wang L, Zhang L. 2006. Succinic semialdehyde couples stress response to quorum-sensing signal decay in Agrobacterium tumefaciens. Mol Microbiol. 62(1):45–56.
  • Wang D, Zheng Y, Wei L, Wei N, Fan X, Huang S, Xiao Q. 2020. A signal-amplified whole-cell biosensor for sensitive detection of Hg2+ based on Hg2+-enhanced reporter module. J Environ Sci (China). 96:93–98.
  • Wenbin N, Dejuan Z, Feifan L, Lei Y, Peng C, Xiaoxuan Y, Hongyu L. 2011. Quorum-sensing system in Acidithiobacillus ferrooxidans involved in its resistance to Cu2. +Lett Appl Microbiol. 53(1):84–91.
  • West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat Rev Microbiol. 4(8):597–607.
  • White C, Sayer J, Gadd G. 1997. Microbial solubilization and immobilization of toxic metals: key biogeochemical processes for treatment of contamination. FEMS Microbiol Rev. 20(3–4):503–516.
  • White P, Claxton L. 2004. Benzo [a] pyrene, polynuclear aromatic compounds, part. Mutat Res. 567(2–3):227–345.
  • Wu Y, Wang C-W, Wang D, Wei N. 2021. A whole-cell biosensor for point-of-care detection of waterborne bacterial pathogens. ACS Synth Biol. 10(2):333–344.
  • Xiong Y, Liu Y. 2012. Essential roles of eDNA and AI-2 in aerobic granulation in sequencing batch reactors operated at different settling times. Appl Microbiol Biotechnol. 93(6):2645–2651.
  • Yan X, Yang J, Wang Q, Lin S. 2021. Transcriptomic analysis reveals resistance mechanisms of Klebsiella michiganensis to copper toxicity under acidic conditions. Ecotoxicol Environ Saf. 211:111919.
  • Yeon KM, Lee CH, Kim J. 2009. Magnetic enzyme carrier for effective biofouling control in the membrane bioreactor based on enzymatic quorum quenching. Environ Sci Technol. 43(19):7403–7409.
  • Yergeau E, Sanschagrin S, Maynard C, St-Arnaud M, Greer CW. 2014. Microbial expression profiles in the rhizosphere of willows depend on soil contamination. ISME J. 8(2):344–358.
  • Yong YC, Yu YY, Li CM, Zhong JJ, Song H. 2011. Bioelectricity enhancement via overexpression of quorum sensing system in Pseudomonas aeruginosa-inoculated microbial fuel cells. Biosens Bioelectron. 30(1):87–92.
  • Yong YC, Zhong JJ. 2010. N-acylated homoserine lactone production and involvement in the biodegradation of aromatics by an environmental isolate of Pseudomonas aeruginosa. Process Biochem. 45(12):1944–1948.
  • Yong YC, Zhong JJ. 2013. Regulation of aromatics biodegradation by rhl quorum sensing system through induction of catechol meta-cleavage pathway. Bioresour Technol. 136:761–765.
  • Zak JC, Willig MR, Moorhead DL, Wildman HG. 1994. Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem. 26(9):1101–1108.
  • Zhang J, Li J, Zhao B, Zhang Y, Wang X, Chen G. 2019. Long-term effects of N-acyl-homoserine lactone-based quorum sensing on the characteristics of ANAMMOX granules in high-loaded reactors. Chemosphere. 218:632–642.
  • Zhao R, Zhang H, Zhang F, Yang F. 2018. Fast start-up anammox process using Acyl-homoserine lactones (AHLs) containing supernatant. J Environ Sci (China). 65:127–132.
  • Zhou P, Mo X, Wang W, Chen X, Lou Y. 2018. The commonly used bactericide bismerthiazol promotes rice defenses against herbivores. Int J Mol Sci. 19(5):1271.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.