Research progress on quorum sensing interference strategies of Salmonella enterica serovar typhimurium

  • XIAO Xue ,
  • ZHANG Hongrui ,
  • ZHANG Peng ,
  • QIAO Jianjun ,
  • CAIYIN Qinggele ,
  • WU Shengbo
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  • 1(School of Chemical Engineering and Technology, Tianjin University, Tianjin 300072, China)
    2(Zhejiang Research Institute of Tianjin University(Shaoxing),Shaoxing 312300, China)
    3(Key Laboratory of Systems Bioengineering, Ministry of Education (Tianjin University), Tianjin 300072, China)
    4(Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin 300072, China)

Received date: 2024-03-20

  Revised date: 2024-05-21

  Online published: 2025-02-14

Abstract

Salmonella enterica serovar Typhimurium is the most common foodborne pathogen, posing a serious threat to public health due to the antibiotic resistance.Recent studies have shown that interference with the quorum sensing (QS) system on pathogens is one of the effective strategies to release their antibiotic resistance.QS is a cell communication mechanism that involves a variety of metabolic activities, such as biofilm formation, motility, virulence factors, adhesion and invasion.In order to systematically summarize the QS mechanisms of S.Typhimurium and its corresponding interference strategies, we firstly introduced five QS systems mediated by N-acyl-homoserine lactones (AHL), autoinducer-2 (AI-2), autoinducer-3 (AI-3), indole and diffusible signaling factor (DSF).Then, we summarized the inhibition and promotion strategies of different QS systems from three aspects:signal molecule synthesis, extracellular transport & reaction, and interaction with receptors.Finally, we pointed out that the future development of QS interference strategies should be based on multi-target and multi-level system networks, which contributes better to solve the infection and the antibiotic resistance of Salmonella.

Cite this article

XIAO Xue , ZHANG Hongrui , ZHANG Peng , QIAO Jianjun , CAIYIN Qinggele , WU Shengbo . Research progress on quorum sensing interference strategies of Salmonella enterica serovar typhimurium[J]. Food and Fermentation Industries, 2025 , 51(2) : 382 -389 . DOI: 10.13995/j.cnki.11-1802/ts.039291

References

[1] DEFOIRDT T.Quorum-sensing systems as targets for antivirulence therapy[J].Trends in Microbiology, 2018, 26(4):313-328.
[2] FAN Q Y, ZUO J, WANG H K, et al.Contribution of quorum sensing to virulence and antibiotic resistance in zoonotic bacteria[J].Biotechnology Advances, 2022, 59:107965.
[3] HAYAT S, MUZAMMIL S, SHABANA, et al.Quorum quenching:Role of nanoparticles as signal jammers in Gram-negative bacteria[J].Future Microbiology, 2019, 14:61-72.
[4] XU Y J, ZENG C L, WEN H Q, et al.Discovery of AI-2 quorum sensing inhibitors targeting the LsrK/HPr protein-protein interaction site by molecular dynamics simulation, virtual screening, and bioassay evaluation[J].Pharmaceuticals, 2023, 16(5):737.
[5] WHITELEY M, DIGGLE S P, GREENBERG E P.Progress in and promise of bacterial quorum sensing research[J].Nature, 2017, 551(7680):313-320.
[6] HABYARIMANA F, SABAG-DAIGLE A, AHMER B M M.The SdiA-regulated gene srgE encodes a type III secreted effector[J].Journal of Bacteriology, 2014, 196(12):2301-2312.
[7] MARQUES J C, OH I K, LY D C, et al.LsrF, a coenzyme A-dependent thiolase, catalyzes the terminal step in processing the quorum sensing signal autoinducer-2[J].Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(39):14235-14240.
[8] MOREIRA C G, WEINSHENKER D, SPERANDIO V.QseC mediates Salmonella enterica serovar typhimurium virulence in vitro and in vivo[J].Infection and Immunity, 2010, 78(3):914-926.
[9] CHOI J, SHIN D, RYU S.Implication of quorum sensing in Salmonella enterica serovar typhimurium virulence:The luxS gene is necessary for expression of genes in pathogenicity island 1[J].Infection and Immunity, 2007, 75(10):4885-4890.
[10] SHARIFI A, NAYERI FASAEI B.Selected plant essential oils inhibit biofilm formation and luxS- and pfs-mediated quorum sensing by Escherichia coli O157:H7[J].Letters in Applied Microbiology, 2022, 74(6):916-923.
[11] HUSNA A U, WANG N, WILKSCH J J, et al.The multifunctional enzyme S-adenosylhomocysteine/methylthioadenosine nucleosidase is a key metabolic enzyme in the virulence of Salmonella enterica var Typhimurium[J].Biochemical Journal, 2019, 476(22):3435-3453.
[12] KHERA R, MEHDIPOUR A R, BOLLA J R, et al.Cryo-EM structures of pentameric autoinducer-2 exporter from Escherichia coli reveal its transport mechanism[J].The EMBO Journal, 2022, 41(18):e109990.
[13] UROZ S, OGER P M, CHAPELLE E, et al.A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases[J].Applied and Environmental Microbiology, 2008, 74(5):1357-1366.
[14] SIO C F, OTTEN L G, COOL R H, et al.Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1[J].Infection and Immunity, 2006, 74(3):1673-1682.
[15] BIJTENHOORN P, MAYERHOFER H, MÜLLER-DIECKMANN J, et al.A novel metagenomic short-chain dehydrogenase/reductase attenuates Pseudomonas aeruginosa biofilm formation and virulence on Caenorhabditis elegans[J].PLoS One, 2011, 6(10):e26278.
[16] ROY V, FERNANDES R, TSAO C Y, et al.Cross species quorum quenching using a native AI-2 processing enzyme[J].ACS Chemical Biology, 2010, 5(2):223-232.
[17] RICE S A, MCDOUGALD D, KUMAR N, et al.The use of quorum-sensing blockers as therapeutic agents for the control of biofilm-associated infections[J].Current Opinion in Investigational Drugs, 2005, 6(2):178-184.
[18] KJELLEBERG S, STEINBERG P, GIVSKOV M, et al.Do marine natural products interfere with prokaryotic AHL regulatory systems?[J].Aquatic Microbial Ecology, 1997, 13:85-93.
[19] JANSSENS J C A, STEENACKERS H, ROBIJNS S, et al.Brominated furanones inhibit biofilm formation by Salmonella enterica serovar Typhimurium[J].Applied and Environmental Microbiology, 2008, 74(21):6639-6648.
[20] LOWERY C A, PARK J, KAUFMANN G F, et al.An unexpected switch in the modulation of AI-2-based quorum sensing discovered through synthetic 4,5-dihydroxy-2,3-pentanedione analogues[J].Journal of the American Chemical Society, 2008, 130(29):9200-9201.
[21] SEMMELHACK M F, CAMPAGNA S R, FEDERLE M J, et al.An expeditious synthesis of DPD and boron binding studies[J].Organic Letters, 2005, 7(4):569-572.
[22] CHOI J, SHIN D, KIM M, et al.LsrR-mediated quorum sensing controls invasiveness of Salmonella typhimurium by regulating SPI-1 and flagella genes[J].PLoS One, 2012, 7(5):e37059.
[23] MOREIRA C G, HERRERA C M, NEEDHAM B D, et al.Virulence and stress-related periplasmic protein (VisP) in bacterial/host associations[J].Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(4):1470-1475.
[24] LI Z, ZHENG Q, XUE X Y, et al.Pyroptosis of Salmonella Typhimurium-infected macrophages was suppressed and elimination of intracellular bacteria from macrophages was promoted by blocking QseC[J].Scientific Reports, 2016, 6:37447.
[25] JI Y, LI W L, ZHANG Y, et al.QseB mediates biofilm formation and invasion in Salmonella enterica serovar Typhi[J].Microbial Pathogenesis, 2017, 104:6-11.
[26] YANG Q, ZOU P Z, CAO Z, et al.QseC Inhibition as a novel antivirulence strategy for the prevention of acute hepatopancreatic necrosis disease (AHPND)-causing Vibrio parahaemolyticus[J].Frontiers in Cellular and Infection Microbiology, 2021, 10:594652.
[27] SNELL E E.Tryptophanase:Structure, catalytic activities, and mechanism of action[J].Advances in Enzymology and Related Areas of Molecular Biology, 1975, 42:287-333.
[28] HAN Y, WANG Y, YU Y M, et al.Indole-Induced reversion of intrinsic multiantibiotic resistance in Lysobacter enzymogenes[J].Applied and Environmental Microbiology, 2017, 83(17):e00995-17.
[29] HIRAKAWA H, INAZUMI Y, MASAKI T, et al.Indole induces the expression of multidrug exporter genes in Escherichia coli[J].Molecular Microbiology, 2005, 55(4):1113-1126.
[30] BAJAJ V, LUCAS R L, HWANG C, et al.Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression[J].Molecular Microbiology, 1996, 22(4):703-714.
[31] LOSTROH C P, LEE C A.The Salmonella pathogenicity island-1 type Ⅲ secretion system[J].Microbes and Infection, 2001, 3(14-15):1281-1291.
[32] LUCAS R L, LOSTROH C P, DIRUSSO C C, et al.Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar typhimurium[J].Journal of Bacteriology, 2000, 182(7):1872-1882.
[33] KOHLI N, CRISP Z, RIORDAN R, et al.The microbiota metabolite indole inhibits Salmonella virulence:Involvement of the PhoPQ two-component system[J].PLoS One, 2018, 13(1):e0190613.
[34] MILLER S I, MEKALANOS J J.Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages[J].Journal of Bacteriology, 1990, 172(5):2485-2490.
[35] SRIDHARAN G V, CHOI K, KLEMASHEVICH C, et al.Prediction and quantification of bioactive microbiota metabolites in the mouse gut[J].Nature Communications, 2014, 5:5492.
[36] GOLUBEVA Y A, ELLERMEIER J R, COTT CHUBIZ J E, et al.Intestinal long-chain fatty acids act as a direct signal to modulate expression of the Salmonella pathogenicity island 1 type Ⅲ secretion system[J].mBio, 2016, 7(1):e02170-15.
[37] HUNG C C, GARNER C D, SLAUCH J M, et al.The intestinal fatty acid propionate inhibits Salmonella invasion through the post-translational control of HilD[J].Molecular Microbiology, 2013, 87(5):1045-1060.
[38] BOSIRE E M, EADE C R, SCHILTZ C J, et al.Diffusible signal factors act through AraC-type transcriptional regulators as chemical cues to repress virulence of enteric pathogens[J].Infection and Immunity, 2020, 88(10):e00226-20.
[39] CHOWDHURY R, PAVINSKI BITAR P D, ADAMS M C, et al.AraC-type regulators HilC and RtsA are directly controlled by an intestinal fatty acid to regulate Salmonella invasion[J].Molecular Microbiology, 2021, 116(6):1464-1475.
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