Review

Salmonella spp. quorum sensing: an overview from environmental persistence to host cell invasion

  • Received: 25 March 2021 Accepted: 22 June 2021 Published: 24 June 2021
  • Salmonella spp. is one of the main foodborne pathogens around the world. It has a cyclic lifestyle that combines host colonization with survival outside the host, implying that Salmonella has to adapt to different conditions rapidly in order to survive. One of these environments outside the host is the food production chain. In this environment, this foodborne pathogen has to adapt to different stress conditions such as acidic environments, nutrient limitation, desiccation, or biocides. One of the mechanisms used by Salmonella to survive under such conditions is biofilm formation. Quorum sensing plays an important role in the production of biofilms composed of cells from the same microorganism or from different species. It is also important in terms of food spoilage and regulates the pathogenicity and invasiveness of Salmonella by regulating Salmonella pathogenicity islands and flagella. Therefore, in this review, we will discuss the genetic mechanism involved in Salmonella quorum sensing, paying special attention to small RNAs and their post-regulatory activity in quorum sensing. We will further discuss the importance of this cell-to-cell communication mechanism in the persistence and spoilage of Salmonella in the food chain environment and the importance in the communication with microorganisms from different species. Subsequently, we will focus on the role of quorum sensing to regulate the virulence and invasion of host cells by Salmonella and on the interaction between Salmonella and other microbial species. This review offers an overview of the importance of quorum sensing in the Salmonella lifestyle.

    Citation: Amanova Sholpan, Alexandre Lamas, Alberto Cepeda, Carlos Manuel Franco. Salmonella spp. quorum sensing: an overview from environmental persistence to host cell invasion[J]. AIMS Microbiology, 2021, 7(2): 238-256. doi: 10.3934/microbiol.2021015

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  • Salmonella spp. is one of the main foodborne pathogens around the world. It has a cyclic lifestyle that combines host colonization with survival outside the host, implying that Salmonella has to adapt to different conditions rapidly in order to survive. One of these environments outside the host is the food production chain. In this environment, this foodborne pathogen has to adapt to different stress conditions such as acidic environments, nutrient limitation, desiccation, or biocides. One of the mechanisms used by Salmonella to survive under such conditions is biofilm formation. Quorum sensing plays an important role in the production of biofilms composed of cells from the same microorganism or from different species. It is also important in terms of food spoilage and regulates the pathogenicity and invasiveness of Salmonella by regulating Salmonella pathogenicity islands and flagella. Therefore, in this review, we will discuss the genetic mechanism involved in Salmonella quorum sensing, paying special attention to small RNAs and their post-regulatory activity in quorum sensing. We will further discuss the importance of this cell-to-cell communication mechanism in the persistence and spoilage of Salmonella in the food chain environment and the importance in the communication with microorganisms from different species. Subsequently, we will focus on the role of quorum sensing to regulate the virulence and invasion of host cells by Salmonella and on the interaction between Salmonella and other microbial species. This review offers an overview of the importance of quorum sensing in the Salmonella lifestyle.



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    Conflict of interest



    The authors declare no conflict of interest.

    Author contributions



    Amanova Sholpan and Alexandre Lamas draft the original manuscript and Alberto Cepeda and Carlos Manuel Franco revised the manuscript. All the authors approved the final version of the manuscript.

    [1] Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, et al. (2014) Supplement 2008–2010 (no. 48) to the White-Kauffmann-Le Minor scheme. Res Microbiol 165: 526-530. doi: 10.1016/j.resmic.2014.07.004
    [2] European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC) (2019) The European Union One Health 2018 Zoonoses Report. EFSA J 17: e05926.
    [3] Lamas A, Miranda JM, Regal P, et al. (2018) A comprehensive review of non-enterica subspecies of Salmonella enterica. Microbiol Res 206: 60-73. doi: 10.1016/j.micres.2017.09.010
    [4] Cox NA, Cason JA, Richardson LJ (2011) Minimization of Salmonella contamination on raw poultry. Annu Rev Food Sci Technol 2: 75-95. doi: 10.1146/annurev-food-022510-133715
    [5] Guillén S, Marcén M, Álvarez I, et al. (2020) Stress resistance of emerging poultry-associated Salmonella serovars. Int J Food Microbiol 335. doi: 10.1016/j.ijfoodmicro.2020.108884
    [6] Arunima A, Swain SK, Ray S, et al. (2020) RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence. Virulence 11: 295-314. doi: 10.1080/21505594.2020.1743540
    [7] Wang H, Huang M, Zeng X, et al. (2020) Resistance profiles of Salmonella isolates exposed to stresses and the expression of small non-coding RNAs. Front Microbiol 11: 130. doi: 10.3389/fmicb.2020.00130
    [8] Dong R, Qin X, He S, et al. (2021) DsrA confers resistance to oxidative stress in Salmonella enterica serovar Typhimurium. Food Control 121.
    [9] Azimi S, Klementiev AD, Whiteley M, et al. (2020) Bacterial quorum sensing during infection. Annu Rev Microbiol 74: 201-219. doi: 10.1146/annurev-micro-032020-093845
    [10] Wu L, Luo Y (2021) Bacterial quorum-sensing systems and their role in intestinal bacteria-host crosstalk. Front Microbiol 12.
    [11] Almeida FAD, Pinto UM, Vanetti MCD (2016) Novel insights from molecular docking of SdiA from Salmonella Enteritidis and Escherichia coli with quorum sensing and quorum quenching molecules. Microb Pathog 99: 178-190. doi: 10.1016/j.micpath.2016.08.024
    [12] Tomasz A (1965) Control of the competent state in pneumococcus by a hormone-like cell product: An example for a new type of regulatory mechanism in bacteria. Nature 208: 155-159. doi: 10.1038/208155a0
    [13] Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104: 313-322. doi: 10.1128/jb.104.1.313-322.1970
    [14] Whiteley M, Diggle SP, Greenberg EP (2017) Progress in and promise of bacterial quorum sensing research. Nature 551: 313-320. doi: 10.1038/nature24624
    [15] Engebrecht J, Nealson K, Silverman M (1983) Bacterial bioluminescence: Isolation and genetic analysis of functions from Vibrio fischeri. Cell 32: 773-781. doi: 10.1016/0092-8674(83)90063-6
    [16] Engebrecht JA, Silverman M (1984) Identification of genes and gene products necessary for bacterial bioluminescence. Proc Natl Acad Sci USA 81: 4154-4158. doi: 10.1073/pnas.81.13.4154
    [17] Eberhard A, Burlingame AL, Eberhard C, et al. (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20: 2444-2449. doi: 10.1021/bi00512a013
    [18] Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: The LuxR-LuxI family of cell density- responsive transcriptional regulators. J Bacteriol 176: 269-275. doi: 10.1128/jb.176.2.269-275.1994
    [19] Williams P, Winzer K, Chan WC, et al. (2007) Look who's talking: Communication and quorum sensing in the bacterial world. Philos Trans R Soc B Biol Sci 362: 1119-1134. doi: 10.1098/rstb.2007.2039
    [20] Skandamis PN, Nychas GE (2012) Quorum sensing in the context of food microbiology. Appl Environ Microbiol 78: 5473-5482. doi: 10.1128/AEM.00468-12
    [21] Boedicker JQ, Vincent ME, Ismagilov RF (2009) Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew Chem Int Ed 48: 5908-5911. doi: 10.1002/anie.200901550
    [22] Smith D, Wang J, Swatton JE, et al. (2007) Variations on a theme: Diverse N-acyl homoserine lactone-mediated quorum sensing mechanisms in Gram-negative bacteria. Sci Prog 89 PART 3: 167-211.
    [23] Winzer K, Hardie KR, Williams P (2003) LuxS and Autoinducer-2: their contribution to quorum sensing and metabolism in bacteria. Adv Appl Microbiol 53.
    [24] Reading NC, Torres AG, Kendall MM, et al. (2007) A novel two-component signaling system that activates transcription of an enterohemorrhagic Escherichia coli effector involved in remodeling of host actin. J Bacteriol 189: 2468-2476. doi: 10.1128/JB.01848-06
    [25] Dunny GM, Leonard BAB (1997) Cell-cell communication in gram-positive bacteria. Annu Rev Microbiol 51: 527-564. doi: 10.1146/annurev.micro.51.1.527
    [26] Lupp C, Urbanowski M, Greenberg EP, et al. (2003) 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 50: 319-331. doi: 10.1046/j.1365-2958.2003.t01-1-03585.x
    [27] Visick KL, Foster J, Doino J, et al. (2000) Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 182: 4578-4586. doi: 10.1128/JB.182.16.4578-4586.2000
    [28] Ahmer BMM, Van Reeuwijk J, Timmers CD, et al. (1998) Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J Bacteriol 180: 1185-1193. doi: 10.1128/JB.180.5.1185-1193.1998
    [29] Patankar AV, González JE (2009) Orphan LuxR regulators of quorum sensing: Review article. FEMS Microbiol Rev 33: 739-756. doi: 10.1111/j.1574-6976.2009.00163.x
    [30] Desai PT, Porwollik S, Long F, et al. (2013) Evolutionary genomics of Salmonella enterica subspecies. mBio 4.
    [31] McQuiston JR, Fields PI, Tauxe RV, et al. (2008) Do Salmonella carry spare tyres? Trends Microbiol 16: 142-148. doi: 10.1016/j.tim.2008.01.009
    [32] Doolittle RF, Feng D, Tsang S, et al. (1996) Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 271: 470-477. doi: 10.1126/science.271.5248.470
    [33] Michael B, Smith JN, Swift S, et al. (2001) SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J Bacteriol 183: 5733-5742. doi: 10.1128/JB.183.19.5733-5742.2001
    [34] Dyszel JL, Smith JN, Lucas DE, et al. (2010) Salmonella enterica serovar typhimurium can detect acyl homoserine lactone production by Yersinia enterocolitica in mice. J Bacteriol 192: 29-37. doi: 10.1128/JB.01139-09
    [35] Nicholson B, David L (2000) DNA methylation-dependent regulation of Pef expression in Salmonella typhimuriumMol Microbiol 35: 728-742. doi: 10.1046/j.1365-2958.2000.01743.x
    [36] Miki T, Okada N, Shimada Y, et al. (2004) Characterization of Salmonella pathogenicity island 1 type III secretion-dependent hemolytic activity in Salmonella enterica serovar Typhimurium. Microb Pathog 37: 65-72. doi: 10.1016/j.micpath.2004.04.006
    [37] Smith JN, Ahmer BMM (2003) Detection of other microbial species by Salmonella: Expression of the SdiA regulon. J Bacteriol 185: 1357-1366. doi: 10.1128/JB.185.4.1357-1366.2003
    [38] Samudrala R, Heffron F, McDermott JE (2009) Accurate prediction of secreted substrates and identification of a conserved putative secretion signal for type iii secretion systems. PLoS Pathog 5: e1000375. doi: 10.1371/journal.ppat.1000375
    [39] Rosselin M, Virlogeux-Payant I, Roy C, et al. (2010) Rck of Salmonella enterica, subspecies enterica serovar Enteritidis, mediates Zipper-like internalization. Cell Res 20: 647-664. doi: 10.1038/cr.2010.45
    [40] Surette MG, Miller MB, Bassler BL (1999) Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: A new family of genes responsible for autoinducer production. Proc Natl Acad Sci USA 96: 1639-1644. doi: 10.1073/pnas.96.4.1639
    [41] Bassler BL, Wright M, Silverman MR (1994) Sequence and function of LuxO, a negative regulator of luminescence in Vibrio harveyiMol Microbiol 12: 403-412. doi: 10.1111/j.1365-2958.1994.tb01029.x
    [42] Pereira CS, Thompson JA, Xavier KB (2013) AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 37: 156-181. doi: 10.1111/j.1574-6976.2012.00345.x
    [43] Taga ME, Bassler BL (2003) Chemical communication among bacteria. Proc Natl Acad Sci USA 100: 14549-14554. doi: 10.1073/pnas.1934514100
    [44] Herzberg M, Kaye IK, Peti W, et al. (2006) YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J Bacteriol 188: 587-598. doi: 10.1128/JB.188.2.587-598.2006
    [45] Xue T, Zhao L, Sun H, et al. (2009) LsrR-binding site recognition and regulatory characteristics in Escherichia coli AI-2 quorum sensing. Cell Res 19: 1258-1268. doi: 10.1038/cr.2009.91
    [46] Pereira CS, Santos AJM, Bejerano-Sagie M, et al. (2012) Phosphoenolpyruvate phosphotransferase system regulates detection and processing of the quorum sensing signal autoinducer-2. Mol Microbiol 84: 93-104. doi: 10.1111/j.1365-2958.2012.08010.x
    [47] Sperandio V, Torres AG, Jarvis B, et al. (2003) Bacteria-host communication: The language of hormones. Proc Natl Acad Sci USA 100: 8951-8956. doi: 10.1073/pnas.1537100100
    [48] Walters M, Sperandio V (2006) Quorum sensing in Escherichia coli and SalmonellaInt J Med Microbiol 296: 125-131. doi: 10.1016/j.ijmm.2006.01.041
    [49] Moreira CG, Sperandio V (2012) Interplay between the qsec and qsee bacterial adrenergic sensor kinases in Salmonella enterica serovar typhimurium pathogenesis. Infect Immun 80: 4344-4353. doi: 10.1128/IAI.00803-12
    [50] Moreira CG, Weinshenker D, Sperandio V (2010) QseC mediates Salmonella enterica serovar typhimurium virulence in vitro and in vivo. Infect Immun 78: 914-926. doi: 10.1128/IAI.01038-09
    [51] Bearson BL, Bearson SMD, Lee IS, et al. (2010) The Salmonella enterica serovar Typhimurium QseB response regulator negatively regulates bacterial motility and swine colonization in the absence of the QseC sensor kinase. Microb Pathog 48: 214-219. doi: 10.1016/j.micpath.2010.03.005
    [52] Clarke MB, Hughes DT, Zhu C, et al. (2006) The QseC sensor kinase: A bacterial adrenergic receptor. Proc Natl Acad Sci USA 103: 10420-10425. doi: 10.1073/pnas.0604343103
    [53] Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136: 615-628. doi: 10.1016/j.cell.2009.01.043
    [54] Mandin P, Guillier M (2013) Expanding control in bacteria: interplay between small RNAs and transcriptional regulators to control gene expression. Curr Opin Microbiol 16: 125-132. doi: 10.1016/j.mib.2012.12.005
    [55] Papenfort K, Vogel J (2010) Regulatory RNA in bacterial pathogens. Cell Host Microbe 8: 116-127. doi: 10.1016/j.chom.2010.06.008
    [56] Papenfort K, Sun Y, Miyakoshi M, et al. (2013) Small RNA-mediated activation of sugar phosphatase mRNA regulates glucose homeostasis. Cell 153: 426-437. doi: 10.1016/j.cell.2013.03.003
    [57] Lenz DH, Mok KC, Lilley BN, et al. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio choleraeCell 118: 69-82. doi: 10.1016/j.cell.2004.06.009
    [58] Hammer BK, Bassler BL (2007) Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio choleraeProc Natl Acad Sci 104: 11145-11149. doi: 10.1073/pnas.0703860104
    [59] Svenningsen SL, Waters CM, Bassler BL (2008) A negative feedback loop involving small RNAs accelerates Vibrio cholerae's transition out of quorum-sensing mode. Genes Dev 22: 226-238. doi: 10.1101/gad.1629908
    [60] Tu KC, Waters CM, Svenningsen SL, et al. (2008) A small-RNA-mediated negative feedback loop controls quorum-sensing dynamics in Vibrio harveyiMol Microbiol 70: 896-907.
    [61] Tu KC, Long T, Svenningsen SL, et al. (2010) Negative feedback loops involving small regulatory RNAs precisely control the Vibrio harveyi quorum-sensing response. Mol Cell 37: 567-579. doi: 10.1016/j.molcel.2010.01.022
    [62] Kay E, Humair B, Dénervaud V, et al. (2006) Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosaJ Bacteriol 188: 6026. doi: 10.1128/JB.00409-06
    [63] Chen R, Wei X, Li Z, et al. (2019) Identification of a small RNA that directly controls the translation of the quorum sensing signal synthase gene rhlI in Pseudomonas aeruginosaEnviron Microbiol 21: 2933-2947. doi: 10.1111/1462-2920.14686
    [64] Malgaonkar A, Nair M (2019) Quorum sensing in Pseudomonas aeruginosa mediated by RhlR is regulated by a small RNA PhrD. Sci Rep 9: 1-11. doi: 10.1038/s41598-018-36488-9
    [65] Li J, Attila C, Wang L, et al. (2007) Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture. J Bacteriol 189: 6011. doi: 10.1128/JB.00014-07
    [66] Arvanitoyannis IS, Stratakos AC (2012) Application of modified atmosphere packaging and active/smart technologies to red meat and poultry: a review. Food Bioprocess Technol 5: 1423-1446. doi: 10.1007/s11947-012-0803-z
    [67] Lamas A, Miranda JM, Vázquez B, et al. (2016) Biofilm formation, phenotypic production of cellulose and gene expression in Salmonella enterica decrease under anaerobic conditions. Int J Food Microbiol 238: 63-67. doi: 10.1016/j.ijfoodmicro.2016.08.043
    [68] Almeida FA, Pimentel-Filho NJ, Pinto UM, et al. (2017) Acyl homoserine lactone-based quorum sensing stimulates biofilm formation by Salmonella Enteritidis in anaerobic conditions. Arch Microbiol 199: 475-486. doi: 10.1007/s00203-016-1313-6
    [69] Carneiro DG, Almeida FA, Aguilar AP, et al. (2020) Salmonella enterica optimizes metabolism after addition of acyl-homoserine lactone under anaerobic conditions. Front Microbiol 11. doi: 10.3389/fmicb.2020.01459
    [70] Donlan RM, Costerton JW (2002) Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15: 167-193. doi: 10.1128/CMR.15.2.167-193.2002
    [71] Ćwiek K, Bugla-Płoskońska G, Wieliczko A (2019) Salmonella biofilm development: Structure and significance. Postepy Hig Med Dosw 73: 937-943. doi: 10.5604/01.3001.0013.7866
    [72] Trampari E, Holden ER, Wickham GJ, et al. (2021) Exposure of Salmonella biofilms to antibiotic concentrations rapidly selects resistance with collateral tradeoffs. npj Biofilms Microbiomes 7. doi: 10.1038/s41522-020-00178-0
    [73] Steenackers H, Hermans K, Vanderleyden J, et al. (2012) Salmonella biofilms: An overview on occurrence, structure, regulation and eradication. Food Res Int 45: 502-531. doi: 10.1016/j.foodres.2011.01.038
    [74] Abraham W (2016) Going beyond the control of quorum-sensing to combat biofilm infections. Antibiotics 5: 3. doi: 10.3390/antibiotics5010003
    [75] Jamuna Bai A, Ravishankar Rai V (2016) Effect of small chain N acyl homoserine lactone quorum sensing signals on biofilms of food-borne pathogens. J Food Sci Technol 53: 3609-3614. doi: 10.1007/s13197-016-2346-1
    [76] Blana V, Georgomanou A, Giaouris E (2017) Assessing biofilm formation by Salmonella enterica serovar Typhimurium on abiotic substrata in the presence of quorum sensing signals produced by Hafnia alveiFood Control 80: 83-91. doi: 10.1016/j.foodcont.2017.04.037
    [77] Campos-Galvão MEM, Ribon AOB, Araújo EF, et al. (2016) Changes in the Salmonella enterica Enteritidis phenotypes in presence of acyl homoserine lactone quorum sensing signals. J Basic Microbiol 56: 493-501. doi: 10.1002/jobm.201500471
    [78] Dourou D, Ammor MS, Skandamis PN, et al. (2011) Growth of Salmonella enteritidis and Salmonella typhimurium in the presence of quorum sensing signalling compounds produced by spoilage and pathogenic bacteria. Food Microbiol 28: 1011-1018. doi: 10.1016/j.fm.2011.02.004
    [79] Yoon Y, Sofos JN (2010) Absence of association of autoinducer-2-based quorum sensing with heat and acid resistance of SalmonellaJ Food Sci 75: M444-M448. doi: 10.1111/j.1750-3841.2010.01744.x
    [80] Solano C, Echeverz M, Lasa I (2014) Biofilm dispersion and quorum sensing. Curr Opin Microbiol 18: 96-104. doi: 10.1016/j.mib.2014.02.008
    [81] Bai AJ, Rai VR (2011) Bacterial quorum sensing and food industry. Compr Rev Food Sci Food Saf 10: 183-193. doi: 10.1111/j.1541-4337.2011.00150.x
    [82] Almasoud A, Hettiarachchy N, Rayaprolu S, et al. (2016) Inhibitory effects of lactic and malic organic acids on autoinducer type 2 (AI-2) quorum sensing of Escherichia coli O157:H7 and Salmonella Typhimurium. LWT-Food Sci Technol 66: 560-564. doi: 10.1016/j.lwt.2015.11.013
    [83] Amrutha B, Sundar K, Shetty PH (2017) Effect of organic acids on biofilm formation and quorum signaling of pathogens from fresh fruits and vegetables. Microb Pathog 111: 156-162. doi: 10.1016/j.micpath.2017.08.042
    [84] Luiz de Freitas L, Aparecida dos Santos CI, Carneiro DG, et al. (2020) Nisin and acid resistance in Salmonella is enhanced by N-dodecanoyl-homoserine lactone. Microb Pathog 147. doi: 10.1016/j.micpath.2020.104320
    [85] Amrutha B, Sundar K, Shetty PH (2017) Spice oil nanoemulsions: Potential natural inhibitors against pathogenic E. coli and Salmonella spp. from fresh fruits and vegetables. LWT-Food Sci Technol 79: 152-159. doi: 10.1016/j.lwt.2017.01.031
    [86] Hakimi Alni R, Ghorban K, Dadmanesh M (2020) Combined effects of Allium sativum and Cuminum cyminum essential oils on planktonic and biofilm forms of Salmonella typhimurium isolates. 3 Biotech 10. doi: 10.1007/s13205-020-02286-2
    [87] Li G, Yan C, Xu YF, et al. (2014) Punicalagin inhibits Salmonella virulence factors and has anti-quorum-sensing potential. Appl Environ Microbiol 80: 6204-6211. doi: 10.1128/AEM.01458-14
    [88] Ma Z, Zhang R, Hai D, et al. (2019) Antibiofilm activity and modes of action of a novel β-sheet peptide against multidrug-resistant Salmonella entericaFood Res Int 125.
    [89] Federle MJ (2009) Autoinducer-2-based chemical communication in bacteria: Complexities of interspecies signaling. Contrib Microbiol 16.
    [90] Jesudhasan PR, Cepeda ML, Widmer K, et al. (2010) Transcriptome analysis of genes controlled by luxS/Autoinducer-2 in Salmonella enterica serovar typhimurium. Foodborne Pathog Dis 7: 399-410. doi: 10.1089/fpd.2009.0372
    [91] Choi J, Shin D, Ryu S (2007) Implication of quorum sensing in Salmonella enterica serovar typhimurium virulence: The luxS gene is necessary for expression of genes in pathogenicity island 1. Infect Immun 75: 4885-4890. doi: 10.1128/IAI.01942-06
    [92] Nesse LL, Berg K, Vestby LK, et al. (2011) Salmonella Typhimurium invasion of HEp-2 epithelial cells in vitro is increased by N-acylhomoserine lactone quorum sensing signals. Acta Vet Scand 53. doi: 10.1186/1751-0147-53-44
    [93] Abed N, Grépinet O, Canepa S, et al. (2014) Direct regulation of the pefI-srgC operon encoding the Rck invasin by the quorum-sensing regulator SdiA in SalmonellaTyphimuriumMol Microbiol 94: 254-271. doi: 10.1111/mmi.12738
    [94] Widmer KW, Jesudhasan P, Pillai SD (2012) Fatty acid modulation of autoinducer (AI-2) influenced growth and macrophage invasion by Salmonella TyphimuriumFoodborne pathog Dis 9: 211-217. doi: 10.1089/fpd.2011.0949
    [95] Smith JN, Dyszel JL, Soares JA, et al. (2008) SdiA, an N-acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS ONE 3.
    [96] Luiz de Freitas L, Pereira da Silva F, Fernandes KM, et al. (2021) The virulence of Salmonella Enteritidis in Galleria mellonella is improved by N-dodecanoyl-homoserine lactone. Microb Pathog 152. doi: 10.1016/j.micpath.2021.104730
    [97] Thompson JA, Oliveira R, Djukovic A, et al. (2015) Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota. Cell Rep 10: 1861-1871. doi: 10.1016/j.celrep.2015.02.049
    [98] Ismail AS, Valastyan JS, Bassler BL (2016) A Host-Produced autoinducer-2 mimic activates bacterial quorum sensing. Cell Host and Microbe 19: 470-480. doi: 10.1016/j.chom.2016.02.020
    [99] Roy V, Fernandes R, Tsao C, et al. (2010) Cross species quorum quenching using a native AI-2 processing enzyme. ACS Chem Biol 5: 223-232. doi: 10.1021/cb9002738
    [100] Hiller CC, Lucca V, Carvalho D, et al. (2019) Influence of catecholamines on biofilm formation by Salmonella EnteritidisMicrob Pathog 130: 54-58. doi: 10.1016/j.micpath.2019.02.032
    [101] Freestone PPE, Haigh RD, Lyte M (2007) Specificity of catecholamine-induced growth in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocoliticaFEMS Microbiol Lett 269: 221-228. doi: 10.1111/j.1574-6968.2006.00619.x
    [102] Pullinger GD, Van Diemen PM, Carnell SC, et al. (2010) 6-hydroxydopamine-mediated release of norepinephrine increases faecal excretion of Salmonella enterica serovar Typhimurium in pigs. Vet Res 41: 68. doi: 10.1051/vetres/2010040
    [103] Dichtl S, Demetz E, Haschka D, et al. (2019) Dopamine is a siderophore-like iron chelator that promotes Salmonella enterica serovar typhimurium virulence in mice. MBio 10. doi: 10.1128/mBio.02624-18
    [104] Lucca V, Borges KA, Furian TQ, et al. (2020) Influence of the norepinephrine and medium acidification in the growth and adhesion of Salmonella Heidelberg isolated from poultry. Microb Pathog 138: 103799. doi: 10.1016/j.micpath.2019.103799
    [105] Reiske L, Schmucker SS, Steuber J, et al. (2020) Interkingdom cross-talk in times of stress: Salmonella Typhimurium grown in the presence of catecholamines inhibits porcine immune functionality in vitroFrontiers in Immunology 11: 2444. doi: 10.3389/fimmu.2020.572056
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