The Transient Multidrug Resistance Phenotype of Salmonella enterica Swarming Cells Is Abolished by Sub-inhibitory Concentrations of Antimicrobial Compounds.

Oihane Irazoki,Jordi Barbé,Susana Campoy

doi:10.3389/fmicb.2017.01360

Oihane Irazoki, Jordi Barbé + Show 1 more

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https://doi.org/10.3389/fmicb.2017.01360

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Abstract

Swarming motility is the rapid and coordinated multicellular migration of bacteria across a moist surface. During swarming, bacterial cells exhibit increased resistance to multiple antibiotics, a phenomenon described as adaptive or transient resistance. In this study, we demonstrate that sub-inhibitory concentrations of cefotaxime, ciprofloxacin, trimethoprim, or chloramphenicol, but not that of amikacin, colistin, kanamycin or tetracycline, impair Salmonella enterica swarming. Chloramphenicol-treated S. enterica cells exhibited a clear decrease in their flagellar content, while treatment with other antibiotics that reduced swarming (cefotaxime, ciprofloxacin, and trimethoprim) inhibited polar chemoreceptor array assembly. Moreover, the increased resistance phenotype acquired by swarming cells was abolished by the presence of these antimicrobials. The same occurred in cells treated with these antimicrobial agents in combination with others that had no effect on swarming motility. Our results reveal the potential of inhibiting swarming ability to enhance the therapeutic effectiveness of antimicrobial agents.

Highlights

Swarming motility is the rapid and coordinated multicellular migration of bacteria across a moist surface mediated by flagella (Henrichsen, 1972)
The effect on swarming of sub-inhibitory concentrations of the following antimicrobial agents differing in their mechanisms of action was analyzed: (i) inhibitors of translation; (ii) an inhibitor of cell-wall synthesis; (iii) an inhibitor of DNA replication; (iv) a disruptor of the outer cell membrane; and (v) an inhibitor of thymidine synthesis
Our results indicated that the presence of kanamycin, amikacin, colistin, and tetracycline did not affect the swarming ability of S. enterica (Figure 1B); rather, the phenotype of the respective bacterial colonies was the same as that of wild-type non-treated cells (Figure 1A)

Summary

Introduction

Swarming motility is the rapid and coordinated multicellular migration of bacteria across a moist surface mediated by flagella (Henrichsen, 1972). Bacterial colonies exhibit a greater resistance to multiple antibiotics when swarming (Kim and Surette, 2003; Kim et al, 2003; Lai et al, 2009; Butler et al, 2010) This adaptive antibiotic resistance has been described for temperate swarmers such as Salmonella enterica, Escherichia coli, and Pseudomonas aeruginosa. In these species, swarmingassociated resistance is non-genetically conferred, since it ceases when the cells are grown under non-swarming conditions (Overhage et al, 2008; Lai et al, 2009; Butler et al, 2010). Multidrug-resistance seems to be a function of the bacterial cell density coupled with the swarming velocity of the bacterial colony (Butler et al, 2010)

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