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Swarming populations ofSalmonella represent a unique physiological state coupled to multiple mechanisms of antibiotic resistance


Salmonella enterica serovar Typhimurium is capable of swarming over semi-solid surfaces. Although its swarming behavior shares many readily observable similarities with other swarming bacteria, the phenomenon remains somewhat of an enigma in this bacterium since some attributes skew away from the better characterized systems. Swarming is quite distinct from the classic swimming motility, as there is a prerequisite for cells to first undergo a morphological transformation into swarmer cells. In some organisms, swarming is controlled by quorum sensing, and in others, swarming has been shown to be coupled to increased expression of important virulence factors. Swarming in serovar Typhimurium is coupled to elevated resistance to a wide variety of structurally and functionally distinct classes of antimicrobial compounds. As serovar Typhimurium differentiates into swarm cells, thepmrHFIJKLM operon is up-regulated, resulting in a more positively charged LPS core. Furthermore, as swarm cells begin to de-differentiate, thepmr operon expression is down-regulated, rapidly reaching the levels observed in swim cells. This is one potential mechanism which confers swarm cells increased resistance to antibiotics such as the cationic antimicrobial peptides. However, additional mechanisms are likely associated with the cells in the swarm state that confer elevated resistance to such a broad spectrum of antimicrobial agents.


  1. 1.

    Finlay BB, Brumell JH.Salmonella interactions with host cells:in vitro toin vivo.PhilTrans R Soc Lond B 2000; 355:623–631.

    Article  CAS  Google Scholar 

  2. 2.

    Finlay BB. Molecular and cellular mechanisms ofSalmonella pathogenesis.Curr Top Microbiol 1994; 192:163–185.

    CAS  Google Scholar 

  3. 3.

    Prouty AM, Schwesinger WH, Gunn JS. Biofilm formation and interaction with the surfaces of gallstones bySalmonella spp.Infect Immun 2002; 70:2640–2649.

    PubMed  Article  CAS  Google Scholar 

  4. 4.

    Berry RM, Armitage JP. The bacterial flagella motor.Adv Microb Physiol 1999; 41:291–337.

    PubMed  Article  CAS  Google Scholar 

  5. 5.

    Bouret RB, Stock AM. Molecular information processing: lessons from bacterial chemotaxis.J Biol Chem 2002;277:9625–9628.

    Article  Google Scholar 

  6. 6.

    Chilcott GS, Hughes KT. Coupling of flagellar gene expression to flagellar assembly inSalmonella enterica serovar Typhimurium andEscherichia coli.Microbiol Mol Biol Rev 2000;64:694–708.

    PubMed  Article  CAS  Google Scholar 

  7. 7.

    Dahlquist FW. Amplification of signaling events in bacteria.Sci STKE 2002; 132:PE24.

    Google Scholar 

  8. 8.

    Stock JB, Surette MG. Chemotaxis. In: Neidhardt FC, Curtis III R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schacchter M, Umbarger HE, editors.Escherichia coli andSalmonella: cellular and molecular biology, 2nd ed. Washington, DC: ASM Press; 1996; p. 1103–1129.

    Google Scholar 

  9. 9.

    Stock JB, Levit MN, Wolanin PM. Information processing in bacterial chemotaxis.Sci STKE 2002; 132:PE25.

    Google Scholar 

  10. 10.

    Harshey RM, Matsuyama T. Dimorphic transition inEscherichia coli andSalmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells.Proc Natl Acad Sci USA 1994; 91:8631–8635.

    PubMed  Article  CAS  Google Scholar 

  11. 11.

    Burkart M, Toguchi A, Harshey RM. The chemotaxis system, but not chemotaxis, is essential for swarming motility inEscherichia coli.Proc Natl Acad Sci USA 1998;95:2568–2573.

    PubMed  Article  CAS  Google Scholar 

  12. 12.

    Fraser GM, Hughes C. Swarming motility.Curr Opin Microbiol 1999; 2:630–635.

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Bassler BL. Small talk. Cell-to-cell communication in bacteria.Cell 2002; 109:421–424.

    PubMed  Article  CAS  Google Scholar 

  14. 14.

    Fuqua C, Parsek MR, Greenberg EP. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing.Ann Rev Genet 2001; 35:439–468.

    PubMed  Article  CAS  Google Scholar 

  15. 15.

    Lindum PW, Anthoni U, Christophersen C, Eberl L, Molin S, Givskov M. N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility ofSerratia liquefaciens MG1.J Bacteriol 1998; 180:6384–6388.

    PubMed  CAS  Google Scholar 

  16. 16.

    Ang S, Horng YT, Shu JC, Soo PC, Liu JH, Yi WC, Lai HC, Luh KT, Ho SW, Swift S. The role of RsmA in the regulation of swarming motility inSerratia marcescens.J Biomed Sci 2001; 8:160–169.

    PubMed  CAS  Google Scholar 

  17. 17.

    Reimman C, Ginet N, Michel L, Keel C, Michaux P, Krishnapillai V, Zala M, Heurlier K, Triandafillu K, Harms destruction reduces virulence gene expression and swarming motility inPseudomonas aeruginosa PAO1.Microbiol 2002; 148:923–932.

    Google Scholar 

  18. 18.

    Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L. Thecep quorum-sensing system ofBurkholderia cepacia H111 controls biofilm formation and swarming motility.Microbiol 2001; 147:2517–2528.

    CAS  Google Scholar 

  19. 19.

    Allison C, Coleman N, Jones PL, Hughes C. Ability ofProteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation.Infect Immun 1992; 60:4740–4746.

    PubMed  CAS  Google Scholar 

  20. 20.

    Fraser GM, Claret L, Furness R, Gupta S, Hughes C. Swarming-coupled expression of theProteus mirabilis hpmBA haemolysin operon.Microbiol 2002; 148:2191–2201.

    CAS  Google Scholar 

  21. 21.

    Kim W, Killam T, Sood V, Surette MG. Swarm-cell differentiation inSalmonella enterica serovar Typhimurium results in elevated resistance to multiple antibiotics.J Bacteriol 2003; 185:3111–3117.

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Bjarnason J, Southward CM, Surette MG. Genomic profiling of iron-responsive genes inSalmonella enterica serovar Typhimurium by high-throughput screening of a random promoter library.J Bacteriol 2003; 185:4973–4982.

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press; 1989.

    Google Scholar 

  24. 24.

    Toguchi A, Siano M, Burkart M, Harshey RM. Genetics of swarming motility inSalmonella enterica serovar Typhimurium: critical role for lipopolysaccharide.J Bacteriol 2000; 182:6308- 6321.

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    Gunn JS, Ryan SS, Van Velkinburgh JC, Ernst RK, Miller SI. Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence ofSalmonella enterica serovar Typhimurium.Infect Immun 2000;68:6139–6146.

    PubMed  Article  CAS  Google Scholar 

  26. 26.

    Trent MS, Ribeiro AA, Lin S, Cotter RJ, Raetz CR. An inner membrane enzyme inSalmonella andEscherichia coli that transfers 4-amino-4-deoxy-L-arabinose to lipid A: induction on polymyxin-resistant mutants and role of a novel lipidlinked donor.J Biol Chem 2001; 276:43122–43131.

    PubMed  Article  CAS  Google Scholar 

  27. 27.

    Brown DF, Brown L. Evaluation of the E test, a novel method of quantifying antimicrobial activity.J Antimicrob Chemother 1991; 27:185–190.

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    Macfarlane ELA, Kwasnicka A, Hancock REW. Role ofPseudomonas aeruginosa PhoP-PhoQ in resistance to antimicrobial cationic peptides and aminoglycosides.Microbiol 2000; 146:2543–2554.

    CAS  Google Scholar 

  29. 29.

    Nichols WW, Dorrington SM, Slack MP, Walmsley HL. Inhibition of tobramycin diffusion by binding to alginate.Antimicrob Agents Chemother 1988; 32:518–523.

    PubMed  CAS  Google Scholar 

  30. 30.

    Brodsky IE, Ernst RK, Miller SI, Falkow S.mig-14 is aSalmonella gene that plays a role in bacterial resistance to antimicrobial peptides.J Bacteriol 2002; 184:3203–3213.

    PubMed  Article  CAS  Google Scholar 

  31. 31.

    Tamayo R, Ryan SS, McCoy AJ, Gunn JS. Identification and genetic characterization of PmrA-regulated genes involved in polymyxin B resistance inSalmonella enterica serovar Typhimurium.Infect Immun 2002; 70:6770–6778.

    PubMed  Article  CAS  Google Scholar 

  32. 32.

    Chow JW. Aminoglycoside resistance in enterococci.Clin Infect Dis 2000; 31:586–589.

    PubMed  Article  CAS  Google Scholar 

  33. 33.

    McCoy AJ, Liu H, Falla TJ, Gunn JS. Identification ofProteus mirabilis mutants with increased sensitivity to antimicrobial peptides.Antimicrob Agents Chemother 2001; 45:2030–2037.

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Stewart PS. Mechanisms of antibiotic resistance in bacterial biofilms.Int J Med Microbiol 2002; 292:107–113.

    PubMed  Article  CAS  Google Scholar 

  35. 35.

    Spoering AL, Lewis K. Biofilms and planktonic cells ofPseudomonas aeruginosa have similar resistance to killing by antimicrobials.J Bacteriol 2001; 183:6746–6751.

    PubMed  Article  CAS  Google Scholar 

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Correspondence to Michael G. Surette.

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Published: September 26, 2003

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Kim, W., Surette, M.G. Swarming populations ofSalmonella represent a unique physiological state coupled to multiple mechanisms of antibiotic resistance. Biol. Proced. Online 5, 189–196 (2003).

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Indexing terms

  • Drug Resistance
  • Salmonella enterica
  • Physiological Processes