1,183
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Quorum sensing modulates bacterial virulence and colonization dynamics of the gastrointestinal pathogen Citrobacter rodentium

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, & ORCID Icon show all
Article: 2267189 | Received 26 Apr 2023, Accepted 02 Oct 2023, Published online: 16 Oct 2023

References

  • Vogt SL, Peña-Díaz J, Finlay BB. Chemical communication in the gut: effects of microbiota-generated metabolites on gastrointestinal bacterial pathogens. Anaerobe. 2015;34:106–19. doi:10.1016/j.anaerobe.2015.05.002.
  • Woodward SE, Krekhno Z, Finlay BB. Here, there, and everywhere: how pathogenic Escherichia coli sense and respond to gastrointestinal biogeography. Cell Microbiol. 2019;21:1–15. doi:10.1111/cmi.13107.
  • Storz G, Hengge R. Bacterial stress responses. 2nd ed. Washington, DC: American Society for Microbiology Press; 2011.
  • Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol. 2001;55:165–199. doi:10.1146/annurev.micro.55.1.165.
  • Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annual review of cell and developmental biology. Annu Rev Cell Dev Biol. 2005;21:319–346. doi:10.1146/annurev.cellbio.21.012704.131001.
  • Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring harbor perspectives in medicine. Cold Spring Harb Perspect Med. 2012;2:a012427. doi:10.1101/cshperspect.a012427.
  • Nealson KH, Hastings JW. Bacterial bioluminescence: its control and ecological significance. Microbiol Rev. 1979;43(4):496–518. doi:10.1128/mr.43.4.496-518.1979.
  • Engebrecht J, Nealson K, Silverman M. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell. 1983;32:773–781. doi:10.1016/0092-8674(83)90063-6.
  • de Kievit TR, Iglewski BH, Portnoy DA. Bacterial quorum sensing in pathogenic relationships. Infect Immun. 2000;68:4839–4849. doi:10.1128/IAI.68.9.4839-4849.2000.
  • Bronesky D, Wu Z, Marzi S, Walter P, Geissmann T, Moreau K, Vandenesch F, Caldelari I, Romby P. Staphylococcus aureus RNAIII and its regulon link quorum sensing, stress responses, metabolic adaptation, and regulation of virulence gene expression. Annu Rev Microbiol. 2016;70:299–316. doi:10.1146/annurev-micro-102215-095708.
  • Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Sci. 1998;280:295–298. doi:10.1126/science.280.5361.295.
  • Hammer BK, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae: biofilms in V. cholerae. Mol Microbiol. 2003;50:101–104. doi:10.1046/j.1365-2958.2003.03688.x.
  • Kong K-F, Vuong C, Otto M. Staphylococcus quorum sensing in biofilm formation and infection. Int J Med Microbiol. 2006;296:133–139. doi:10.1016/j.ijmm.2006.01.042.
  • Fuqua C, Parsek MR, Greenberg EP. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet. 2001;35:439–468. doi:10.1146/annurev.genet.35.102401.090913.
  • Papenfort K, Bassler BL. Quorum sensing signal–response systems in gram-negative bacteria. Nat Rev Microbiol. 2016;14:576–588. doi:10.1038/nrmicro.2016.89.
  • von Bodman SB, Willey JM, Diggle SP. Cell-cell communication in bacteria: united we stand. J Bacteriol. 2008;190:4377–4391. doi:10.1128/JB.00486-08.
  • Swearingen MC, Sabag-Daigle A, Ahmer BMM. Are there acyl-homoserine lactones within mammalian intestines? J Bacteriol. 2013;195:173–179. doi:10.1128/JB.01341-12.
  • Thompson JA, Oliveira R, Djukovic A, Ubeda C, Xavier KB. Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota. Cell Rep. 2015;10:1861–1871. doi:10.1016/j.celrep.2015.02.049.
  • Coquant G, Grill J-P, Seksik P. Impact of N-Acyl-homoserine lactones, quorum sensing molecules, on gut immunity. Front Immunol. 2020;11:1827. doi:10.3389/fimmu.2020.01827.
  • Coquant G, Aguanno D, Brot L, Belloir C, Delugeard J, Roger N, Pham H-P, Briand L, Moreau M, de Sordi L, et al. 3-oxo-C12: 2-HSL, quorum sensing molecule from human intestinal microbiota, inhibits pro-inflammatory pathways in immune cells via bitter taste receptors. Sci Rep. 2022;12(12):9440. doi:10.1038/s41598-022-13451-3.
  • Hsiao A, Ahmed AMS, Subramanian S, Griffin NW, Drewry LL, Petri WA, Haque R, Ahmed T, Gordon JI. Members of the human gut microbiota involved in recovery from Vibrio cholerae infection. Nature. 2014;515:423–426. doi:10.1038/nature13738.
  • Collins JW, Keeney KM, Crepin VF, Rathinam VAK, Fitzgerald KA, Finlay BB, Frankel G. Citrobacter rodentium: infection, inflammation and the microbiota. Nat Rev Microbiol. 2014;12:612–623. doi:10.1038/nrmicro3315.
  • Crepin VF, Collins JW, Habibzay M, Frankel G. Citrobacter rodentium mouse model of bacterial infection. Nat Protoc. 2016;11:1851–1876. doi:10.1038/nprot.2016.100.
  • Schauer DB, Falkow S. Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect Immun. 1993;61:2486–2492. doi:10.1128/iai.61.6.2486-2492.1993.
  • Deng W, Vallance BA, Li Y, Puente JL, Finlay BB. Citrobacter rodentium translocated intimin receptor (Tir) is an essential virulence factor needed for actin condensation, intestinal colonization and colonic hyperplasia in mice. Mol Microbiol. 2003;48:95–115. doi:10.1046/j.1365-2958.2003.03429.x.
  • McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA. 1995;92:1664–1668. doi:10.1073/pnas.92.5.1664.
  • Deng W, Li Y, Vallance BA, Finlay BB, O’Brien AD. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect Immun. 2001;69:6323–6335. doi:10.1128/IAI.69.10.6323-6335.2001.
  • Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, Vázquez A, Barba J, Ibarra JA, O’Donnell P, Metalnikov P, Ashman, K., et al. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA. 2004;101:3597–3602. doi:10.1073/pnas.0400326101.
  • Coulthurst SJ, Clare S, Evans TJ, Foulds IJ, Roberts KJ, Welch M, Dougan G, Salmond GPC. Quorum sensing has an unexpected role in virulence in the model pathogen Citrobacter rodentium. EMBO Rep. 2007;8(7):698–703. doi:10.1038/sj.embor.7400984.
  • Hense BA, Schuster M. Core principles of bacterial autoinducer systems. Microbiol Mol Biol Rev. 2015;79(1):153–169. doi:10.1128/MMBR.00024-14.
  • Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. 2010. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
  • Dong T, Schellhorn HE. Role of RpoS in virulence of pathogens. Infect Immun. 2010;78(3):887–897. doi:10.1128/IAI.00882-09.
  • Spratt MR, Lane K, Dunlop M, Yount J. Navigating environmental transitions: the role of phenotypic variation in bacterial responses. mBio. 2022;13(6):e02212–22. doi:10.1128/mbio.02212-22.
  • Contijoch EJ, Britton GJ, Yang C, Mogno I, Li Z, Ng R, Llewellyn SR, Hira S, Johnson C, Rabinowitz KM, et al. Gut microbiota density influences host physiology and is shaped by host and microbial factors. eLife. 2019;8:e40553. doi:10.7554/eLife.40553.
  • Woodward SE, Vogt SL, Peña-Díaz J, Melnyk RA, Cirstea M, Serapio-Palacios A, Neufeld LMP, Huus KE, Wang MA, Haney CH, et al. Gastric acid and escape to systemic circulation represent major bottlenecks to host infection by Citrobacter rodentium. ISME J. 2023;17(1):36–46. doi:10.1038/s41396-022-01321-9.
  • Vallance BA, Deng W, Jacobson K, Finlay BB. Host susceptibility to the Attaching and effacing bacterial pathogen Citrobacter rodentium. Infect Immun. 2003;71(6):3443–3453. doi:10.1128/IAI.71.6.3443-3453.2003.
  • Guttman JA, Li Y, Wickham ME, Deng W, Vogl AW, Finlay BB. Attaching and effacing pathogen-induced tight junction disruption in vivo. Cell Microbiol. 2006;8(4):634–645. doi:10.1111/j.1462-5822.2005.00656.x.
  • Dyszel JL, Smith JN, Lucas DE, Soares JA, Swearingen MC, Vross MA, Young GM, Ahmer BMM. Salmonella enterica serovar typhimurium can detect acyl homoserine lactone production by Yersinia enterocolitica in mice. J Bacteriol. 2010;192(1):29–37. doi:10.1128/JB.01139-09.
  • Landman C, Grill J-P, Mallet J-M, Marteau P, Humbert L, Le Balc’h E, Maubert M-A, Perez K, Chaara W, Brot L, et al. Inter-kingdom effect on epithelial cells of the N-Acyl homoserine lactone 3-oxo-C12: 2, a major quorum-sensing molecule from gut microbiota. PLoS One. 2018;13(8):e0202587. doi:10.1371/journal.pone.0202587.
  • Xue J, Chi L, Tu P, Lai Y, Liu C-W, Ru H, Lu K. Detection of gut microbiota and pathogen produced N-acyl homoserine in host circulation and tissues. NPJ Biofilms Microbio. 2021;7(1):53. 10.1038/s41522-021-00224–5. doi:10.1038/s41522-021-00224-5.
  • Kim MK, Ingremeau F, Zhao A, Bassler BL, Stone HA. Local and global consequences of flow on bacterial quorum sensing. Nat microbiol. 2016;1(1):15005. doi:10.1038/nmicrobiol.2015.5.
  • Siryaporn A, Kim MK, Shen Y, Stone HA, Gitai Z. Colonization, competition, and dispersal of pathogens in fluid flow networks. Curr Biol. 2015;25(9):1201–1207. doi:10.1016/j.cub.2015.02.074.
  • Thomson NR, Crow MA, McGowan SJ, Cox A, Salmond GPC. Biosynthesis of carbapenem antibiotic and prodigiosin pigment in serratia is under quorum sensing control: production of antibiotic and pigment by serratia. Mol Microbiol. 2002;36(3):539–556. doi:10.1046/j.1365-2958.2000.01872.x.
  • Ortori CA, Atkinson S, Chhabra SR, Cámara M, Williams P, Barrett DA. Comprehensive profiling of N-acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole–linear ion trap mass spectrometry. Anal Bioanal Chem. 2007;387(2):497–511. doi:10.1007/s00216-006-0710-0.
  • Gould TA, Herman J, Krank J, Murphy RC, Churchill MEA. Specificity of acyl-homoserine lactone synthases examined by mass spectrometry. J Bacteriol. 2006;188(2):773–783. doi:10.1128/JB.188.2.773-783.2006.
  • Montebello AN, Brecht RM, Turner RD, Ghali M, Pu X, Nagarajan R. Acyl-ACP substrate recognition in Burkholderia mallei BmaI1 acyl-homoserine lactone synthase. Biochemistry. 2014;53(39):6231–6242. doi:10.1021/bi5009529.
  • Arnoldini M, Vizcarra IA, Peña-Miller R, Stocker N, Diard M, Vogel V, Beardmore RE, Hardt W-D, Ackermann M, Balaban N. Bistable expression of virulence genes in salmonella leads to the formation of an antibiotic-tolerant subpopulation. PLoS Biol. 2014;12(8):e1001928. doi:10.1371/journal.pbio.1001928.
  • Gorelik O, Levy N, Shaulov L, Yegodayev K, Meijler MM, Sal-Man N. Vibrio cholerae autoinducer-1 enhances the virulence of enteropathogenic Escherichia coli. Sci Rep. 2019;9(1):4122. doi:10.1038/s41598-019-40859-1.
  • Subramoni S, Venturi V. LuxR-family ‘solos’: bachelor sensors/regulators of signalling molecules. Microbiology. 2009;155(5):1377–1385. doi:10.1099/mic.0.026849-0.
  • Whiteley M, Diggle SP, Greenberg EP. Progress in and promise of bacterial quorum sensing research. Nature. 2017;551(7680):313–320. doi:10.1038/nature24624.
  • Paluch E, Rewak-Soroczyńska J, Jędrusik I, Mazurkiewicz E, Jermakow K. Prevention of biofilm formation by quorum quenching. Appl Microbiol Biotechnol. 2020;104(5):1871–1881. doi:10.1007/s00253-020-10349-w.
  • Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA. 2002;99(5):3129–3134. doi:10.1073/pnas.052694299.
  • Bridges AA, Bassler BL, Sourjik V. The intragenus and interspecies quorum-sensing autoinducers exert distinct control over Vibrio cholerae biofilm formation and dispersal. PLoS Biol. 2019;17(11):e3000429. doi:10.1371/journal.pbio.3000429.
  • Krzyżek P. Challenges and limitations of anti-quorum sensing therapies. Front Microbiol. 2019;10:2473. doi:10.3389/fmicb.2019.02473.
  • Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6(5):343–345. doi:10.1038/nmeth.1318.
  • Ferriéres L, Hémery G, Nham T, Guérout AM, Mazel D, Beloin C, Ghigo JM. Silent mischief: bacteriophage mu insertions contaminate products of Escherichia coli random mutagenesis performed using suicidal transposon delivery plasmids mobilized by broad-host-range RP4 conjugative machinery. J Bacteriol. 2010;192(24):6418–6427. doi:10.1128/JB.00621-10.
  • Donnenberg MS, Kaper JB. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun. 1991;59(12):4310–4317. doi:10.1128/iai.59.12.4310-4317.1991.
  • Choi KH, Schweizer HP. Mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc. 2006;1(1):153–161. doi:10.1038/nprot.2006.24.
  • Duncan SH, Hold GL, Harmsen HJM, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol. 2002;52(6):2141–2146. doi:10.1099/00207713-52-6-2141.
  • Shaw PD, Ping G, Daly SL, Cha C, Cronan JE, Rinehart KL, Farrand SK. Detecting and characterizing N -acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci USA. 1997;94(12):6036–6041. doi:10.1073/pnas.94.12.6036.
  • Zhu J, Beaber JW, Moré MI, Fuqua C, Eberhard A, Winans SC. Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of agrobacterium tumefaciens. J Bacteriol. 1998;180(20):5398–5405. doi:10.1128/JB.180.20.5398-5405.1998.
  • Bhagwat AA, Ying ZI, Karns J, Smith A. Determining RNA quality for NextGen sequencing: some exceptions to the gold standard rule of 23S to 16S rRNA ratio§. Microbiol Discov. 2013;1(1):10. doi:10.7243/2052-6180-1-10.
  • Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. doi:10.1093/bioinformatics/bts635.
  • Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32(19):3047–3048. doi:10.1093/bioinformatics/btw354.
  • Wang L, Wang S, Li W. RSeQC: quality control of RNA-seq experiments. Bioinformatics. 2012;28(16):2184–2185. doi:10.1093/bioinformatics/bts356.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi:10.1186/s13059-014-0550-8.
  • Ignatiadis N, Klaus B, Zaugg JB, Huber W. Data-driven hypothesis weighting increases detection power in genome-scale multiple testing. Nat Methods. 2016;13(7):577–580. doi:10.1038/nmeth.3885.
  • Zhu A, Ibrahim JG, Love MI, Stegle O. Heavy-tailed prior distributions for sequence count data: removing the noise and preserving large differences. Bioinformatics. 2019;35(12):2084–2092. doi:10.1093/bioinformatics/bty895.
  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov, J P., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545–15550. doi:10.1073/pnas.0506580102.
  • Mootha VK, Lindgren CM, Eriksson K-F, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003;34(3):267–273. doi:10.1038/ng1180.
  • Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, Feng T, Zhou L, Tang W, Zhan L, et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innov. 2021;2(3):100141. doi:10.1016/j.xinn.2021.100141.
  • Taylor SC, Nadeau K, Abbasi M, Lachance C, Nguyen M, Fenrich J. The ultimate qPCR Experiment: producing publication quality, reproducible data the first time. Trends Biotechnol. 2019;37(7):761–774. doi:10.1016/j.tibtech.2018.12.002.