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Limited impact of Salmonella stress and persisters on antibiotic clearance

  • Bjarnsholt, T. et al. The importance of understanding the infectious microenvironment. Lancet Infect. Dis. 22, e88–e92 (2022).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Balaban, N. Q. et al. Definitions and guidelines for research on antibiotic persistence. Nat. Rev. Microbiol. 17, 441–448 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Claudi, B. et al. Phenotypic variation of Salmonella in host tissues delays eradication by antimicrobial chemotherapy. Cell 158, 722–733 (2014).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Cunrath, O. & Bumann, D. Host resistance factor SLC11A1 restricts Salmonella growth through magnesium deprivation. Science 366, 995–999 (2019).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Steeb, B. et al. Parallel exploitation of diverse host nutrients enhances Salmonella virulence. PLoS Pathog. 9, e1003301 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Doern, G. V. & Brecher, S. M. The clinical predictive value (or lack thereof) of the results of in vitro. J. Clin. Microbiol. 49, S11–S14 (2011).

    Article 
    PubMed Central 
    MATH 

    Google Scholar
     

  • WHO Bacterial Priority Pathogens List, 2024: Bacterial Pathogens of Public Health Importance, to Guide Research, Development and Strategies to Prevent and Control Antimicrobial Resistance (World Health Organization, 2024).

  • Newson, J. P., Gaissmaier, M. S., McHugh, S. C. & Hardt, W. D. Studying antibiotic persistence in vivo using the model organism Salmonella Typhimurium. Curr. Opin. Microbiol. 70, 102224 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bumann, D. Heterogeneous host-pathogen encounters: act locally, think globally. Cell Host Microbe 17, 13–19 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fang, F. C., Frawley, E. R., Tapscott, T. & Vazquez-Torres, A. Bacterial stress responses during host infection. Cell Host Microbe 20, 133–143 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu, X. et al. Pharmacokinetics and pharmacodynamics of enrofloxacin treatment of Escherichia coli in a murine thigh infection modeling. BMC Vet. Res. 17, 212 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Li, J. et al. Tissue compartmentalization enables Salmonella persistence during chemotherapy. Proc. Natl Acad. Sci. USA 118, e2113951118 (2021).

  • Dobinson, H. C. et al. Evaluation of the clinical and microbiological response to Salmonella Paratyphi A infection in the first paratyphoid human challenge model. Clin. Infect. Dis. 64, 1066–1073 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Wang, E., Bergeron, Y. & Bergeron, M. G. Ceftriaxone pharmacokinetics in interleukin-10-treated murine pneumococcal pneumonia. J. Antimicrob. Chemother. 55, 721–726 (2005).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Dorr, T., Lewis, K. & Vulic, M. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet. 5, e1000760 (2009).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Dorr, T., Vulic, M. & Lewis, K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 8, e1000317 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Helaine, S. et al. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 343, 204–208 (2014).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Pontes, M. H. & Groisman, E. A. Slow growth determines nonheritable antibiotic resistance in Salmonella enterica. Sci. Signal. 12, eaax3938 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, S. et al. Contribution of target gene mutations and efflux to decreased susceptibility of Salmonella enterica serovar typhimurium to fluoroquinolones and other antimicrobials. Antimicrob. Agents Chemother. 51, 535–542 (2007).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Bergmiller, T. et al. Biased partitioning of the multidrug efflux pump AcrAB–TolC underlies long-lived phenotypic heterogeneity. Science 356, 311–315 (2017).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Aldridge, B. B. et al. Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science 335, 100–104 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Kaldalu, N. & Tenson, T. Slow growth causes bacterial persistence. Sci. Signal. 12, eaay1167 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Rotem, E. et al. Regulation of phenotypic variability by a threshold-based mechanism underlies bacterial persistence. Proc. Natl Acad. Sci. USA 107, 12541–12546 (2010).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Korch, S. B., Henderson, T. A. & Hill, T. M. Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol. Microbiol. 50, 1199–1213 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lopatkin, A. J. et al. Bacterial metabolic state more accurately predicts antibiotic lethality than growth rate. Nat. Microbiol. 4, 2109–2117 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tuomanen, E., Cozens, R., Tosch, W., Zak, O. & Tomasz, A. The rate of killing of Escherichia coli by beta-lactam antibiotics is strictly proportional to the rate of bacterial growth. J. Gen. Microbiol. 132, 1297–1304 (1986).

    CAS 
    PubMed 

    Google Scholar
     

  • Aldred, K. J., Kerns, R. J. & Osheroff, N. Mechanism of quinolone action and resistance. Biochemistry 53, 1565–1574 (2014).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Wiktor, J. et al. RecA finds homologous DNA by reduced dimensionality search. Nature 597, 426–429 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Amarh, V., White, M. A. & Leach, D. R. F. Dynamics of RecA-mediated repair of replication-dependent DNA breaks. J. Cell Biol. 217, 2299–2307 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lesterlin, C., Ball, G., Schermelleh, L. & Sherratt, D. J. RecA bundles mediate homology pairing between distant sisters during DNA break repair. Nature 506, 249–253 (2014).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Renzette, N. et al. Localization of RecA in Escherichia coli K-12 using RecA-GFP. Mol. Microbiol. 57, 1074–1085 (2005).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Azevedo, N. F. et al. Proposal for a method to estimate nutrient shock effects in bacteria. BMC Res. Notes 5, 422 (2012).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Wiedemann, B. & Kratz, B. in Ciprofloxacin iv. Defining its Role in Serious Infection (ed. Garrard, C.) 13–19 (Springer, 1993).

  • Mok, W. W. K. & Brynildsen, M. P. Timing of DNA damage responses impacts persistence to fluoroquinolones. Proc. Natl Acad. Sci. USA 115, E6301–e6309 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Pontes, M. H. & Groisman, E. A. A physiological basis for nonheritable antibiotic resistance. mBio 11, e00817–e00820 (2020).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Norman, A., Hestbjerg Hansen, L. & Sorensen, S. J. Construction of a ColD cda promoter-based SOS–green fluorescent protein whole-cell biosensor with higher sensitivity toward genotoxic compounds than constructs based on recA, umuDC, or sulA promoters. Appl. Environ. Microbiol. 71, 2338–2346 (2005).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Malik, M., Hussain, S. & Drlica, K. Effect of anaerobic growth on quinolone lethality with Escherichia coli. Antimicrob. Agents Chemother. 51, 28–34 (2007).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Hoiseth, S. K. & Stocker, B. A. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291, 238–239 (1981).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Michaux, C., Ronneau, S., Giorgio, R. T. & Helaine, S. Antibiotic tolerance and persistence have distinct fitness trade-offs. PLoS Pathog. 18, e1010963 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Slattery, A., Victorsen, A. H., Brown, A., Hillman, K. & Phillips, G. J. Isolation of highly persistent mutants of Salmonella enterica serovar typhimurium reveals a new toxin–antitoxin module. J. Bacteriol. 195, 647–657 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stapels, D. A. C. et al. Salmonella persisters undermine host immune defenses during antibiotic treatment. Science 362, 1156–1160 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Slate, A. R. et al. Efficacy of enrofloxacin in a mouse model of sepsis. J. Am. Assoc. Lab. Anim. Sci. 53, 381–386 (2014).

    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Griffin, A. J., Li, L. X., Voedisch, S., Pabst, O. & McSorley, S. J. Dissemination of persistent intestinal bacteria via the mesenteric lymph nodes causes typhoid relapse. Infect. Immun. 79, 1479–1488 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jurėnas, D., Fraikin, N., Goormaghtigh, F. & Van Melderen, L. Biology and evolution of bacterial toxin–antitoxin systems. Nat. Rev. Microbiol. 20, 335–350 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • LeRoux, M. & Laub, M. T. Toxin–antitoxin systems as phage defense elements. Annu. Rev. Microbiol. 76, 21–43 (2022).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Ryall, B., Eydallin, G. & Ferenci, T. Culture history and population heterogeneity as determinants of bacterial adaptation: the adaptomics of a single environmental transition. Microbiol. Mol. Biol. Rev. 76, 597–625 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Ciolli Mattioli, C. et al. Physiological stress drives the emergence of a Salmonella subpopulation through ribosomal RNA regulation. Curr. Biol. 33, 4880–4892.e14 (2023).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Woodward, W. E. Volunteer studies of typhoid fever and vaccines. Trans. R. Soc. Trop. Med. Hyg. 74, 553–556 (1980).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Kaiser, P. et al. Cecum lymph node dendritic cells harbor slow-growing bacteria phenotypically tolerant to antibiotic treatment. PLoS Biol. 12, e1001793 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Giesbrecht, P., Kersten, T., Maidhof, H. & Wecke, J. Staphylococcal cell wall: morphogenesis and fatal variations in the presence of penicillin. Microbiol. Mol. Biol. Rev. 62, 1371–1414 (1998).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Davoodi, S., Daryaee, F., Chang, A., Walker, S. G. & Tonge, P. J. Correlating drug-target residence time and post-antibiotic effect: insight into target vulnerability. ACS Infect. Dis. 6, 629–636 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • MacKenzie, F. M. & Gould, I. M. The post-antibiotic effect. J. Antimicrob. Chemother. 32, 519–537 (1993).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Grant, J. & Saux, N. L. Duration of antibiotic therapy for common infections. J. Assoc. Med. Microbiol. Infect. Dis. Can. 6, 181–197 (2021).

    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Awofisayo-Okuyelu, A., McCarthy, N., Mgbakor, I. & Hall, I. Incubation period of typhoidal salmonellosis: a systematic review and meta-analysis of outbreaks and experimental studies occurring over the last century. BMC Infect. Dis. 18, 483 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Behr, M. A., Edelstein, P. H. & Ramakrishnan, L. Revisiting the timetable of tuberculosis. BMJ 362, k2738 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Smit, J. et al. Onset of symptoms, diagnostic confirmation, and occurrence of multiple infective foci in patients with Staphylococcus aureus bloodstream infection: a look into the order of events and potential clinical implications. Infection 46, 651–658 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Hasanjani Roushan, M. R. & Ebrahimpour, S. Human brucellosis: an overview. Caspian J. Intern. Med. 6, 46–47 (2015).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kroger, C. et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc. Natl Acad. Sci. USA 109, E1277–E1286 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bunny, K., Liu, J. & Roth, J. Phenotypes of lexA mutations in Salmonella enterica: evidence for a lethal lexA null phenotype due to the Fels-2 prophage. J. Bacteriol. 184, 6235–6249 (2002).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Craig, M. & Slauch, J. M. Phagocytic superoxide specifically damages an extracytoplasmic target to inhibit or kill Salmonella. PLoS ONE 4, e4975 (2009).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rollenhagen, C., Sorensen, M., Rizos, K., Hurvitz, R. & Bumann, D. Antigen selection based on expression levels during infection facilitates vaccine development for an intracellular pathogen. Proc. Natl Acad. Sci. USA 101, 8739–8744 (2004).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Roos, U., Harkness, R. E. & Braun, V. Assembly of colicin genes from a few DNA fragments. Nucleotide sequence of colicin D. Mol. Microbiol. 3, 891–902 (1989).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Hofinger, C., Karch, H. & Schmidt, H. Structure and function of plasmid pColD157 of enterohemorrhagic Escherichia coli O157 and its distribution among strains from patients with diarrhea and hemolytic–uremic syndrome. J. Clin. Microbiol. 36, 24–29 (1998).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rollenhagen, C. & Bumann, D. Salmonella enterica highly expressed genes are disease specific. Infect. Immun. 74, 1649–1660 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cianfanelli, F. R., Cunrath, O. & Bumann, D. Efficient dual-negative selection for bacterial genome editing. BMC Microbiol. 20, 129 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nanchen, A., Schicker, A. & Sauer, U. Nonlinear dependency of intracellular fluxes on growth rate in miniaturized continuous cultures of Escherichia coli. Appl. Environ. Microbiol. 72, 1164–1172 (2006).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • de Jong, N. W., van der Horst, T., van Strijp, J. A. & Nijland, R. Fluorescent reporters for markerless genomic integration in Staphylococcus aureus. Sci. Rep. 7, 43889 (2017).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Burian, M. et al. Temporal expression of adhesion factors and activity of global regulators during establishment of Staphylococcus aureus nasal colonization. J. Infect. Dis. 201, 1414–1421 (2010).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Burton, N. A. et al. Disparate impact of oxidative host defenses determines the fate of Salmonella during systemic infection in mice. Cell Host Microbe 15, 72–83 (2014).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thévenaz, P., Ruttimann, U. E. & Unser, M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27–41 (1998).

    Article 
    ADS 
    PubMed 
    MATH 

    Google Scholar
     

  • Becker, D. et al. Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 440, 303–307 (2006).

    Article 
    ADS 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Volkmer, B. & Heinemann, M. Condition-dependent cell volume and concentration of Escherichia coli to facilitate data conversion for systems biology modeling. PLoS ONE 6, e23126 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

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