Better together–Salmonella biofilm-associated antibiotic resistance

References

• Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, Praet N, Bellinger DC, de Silva NR, Gargouri N, et al. World health organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med. 2015;12(12):e1001923. doi:10.1371/journal.pmed.1001923.
   PubMed Web of Science ®Google Scholar
• Ryan MP, O’Dwyer J, Adley CC. Evaluation of the complex nomenclature of the clinically and veterinary significant pathogen Salmonella. Biomed Res Int. 2017;2017 doi:10.1155/2017/3782182.
   Web of Science ®Google Scholar
• Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesús J, Platt DJ, Olsen JE. Host adapted serotypes of Salmonella enterica. Epidemiol Infect. 2000;125(2):229–22. doi:10.1017/S0950268899004379.
   PubMed Web of Science ®Google Scholar
• Zhang S, Kingsley RA, Santos RL, Andrews-Polymenis H, Raffatellu M, Figueiredo J, Nunes J, Tsolis RM, Adams LG, Bäumler AJ, et al. Molecular pathogenesis of Salmonella enterica serotype typhimurium-induced diarrhea. Infect Immun. 2003;71(1):1–12. doi:10.1128/IAI.71.1.1-12.2003.
   PubMed Web of Science ®Google Scholar
• Gal-Mor O. Persistent infection and long-term carriage of typhoidal and nontyphoidal salmonellae. Clin Microbiol Rev. 2019;32(1). doi:10.1128/CMR.00088-18.
   PubMed Web of Science ®Google Scholar
• European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J. 2018;16(12). doi:10.2903/j.efsa.2018.5500.
   Web of Science ®Google Scholar
• Vandenberg O, Nyarukweba DZ, Ndeba PM, Hendriksen RS, Barzilay EJ, Schirvel C, Bisimwa BB, Collard J-M, Aidara Kane A, Aarestrup FM, et al. Microbiologic and clinical features of salmonella species isolated from bacteremic children in eastern democratic republic of congo. Pediatr Infect Dis J. 2010;29(6):504–510. doi:10.1097/INF.0b013e3181cd615a.
   PubMed Web of Science ®Google Scholar
• Costerton JW, Geesey GG, Cheng KJ. How bacteria stick. Sci Am. 1978;238(1):86–95. doi:10.1038/scientificamerican0178-86.
   PubMed Web of Science ®Google Scholar
• Harrell JE, Hahn MM, D’Souza SJ, Vasicek EM, Sandala JL, Gunn JS, McLachlan JB. Salmonella biofilm formation, chronic infection, and immunity within the intestine and hepatobiliary tract. Front Cell Infect Microbiol. 2021;10. doi:10.3389/fcimb.2020.624622.
   PubMed Web of Science ®Google Scholar
• Landini P, Antoniani D, Burgess JG, Nijland R. Molecular mechanisms of compounds affecting bacterial biofilm formation and dispersal. Appl Microbiol Biotechnol. 2010;86(3):813–823. Preprint at. doi:10.1007/s00253-010-2468-8.
   PubMed Web of Science ®Google Scholar
• Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8(9):623–633. doi:10.1038/nrmicro2415.
   PubMed Web of Science ®Google Scholar
• Holden ER, Yasir M, Turner AK, Charles IG, Webber MA. Comparison of the genetic basis of biofilm formation between Salmonella Typhimurium and Escherichia coli. Microb Genom. 2022;8(11). doi:10.1099/mgen.0.000885.
   PubMed Web of Science ®Google Scholar
• De la Fuente-Núñez C, Reffuveille F, Fernández L, Hancock REW. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol. 2013;16(5):580–589. doi:10.1016/j.mib.2013.06.013.
   PubMed Web of Science ®Google Scholar
• Mah TF. Biofilm-specific antibiotic resistance. Future Microbiol. 2012;7(9):1061–1072. doi:10.2217/fmb.12.76.
   PubMed Web of Science ®Google Scholar
• Tursi SA, Tükel Ç. Curli-containing enteric biofilms inside and out: matrix composition, immune recognition, and disease implications. Microbiol Mol Biol R. 2018;82(4). doi:10.1128/MMBR.00028-18.
   PubMed Web of Science ®Google Scholar
• Percival SL, Suleman L, Vuotto C, Donelli G. Healthcare-associated infections, medical devices and biofilms: risk, tolerance and control. J Med Microbiol. 2015;64(4):323–334. doi:10.1099/jmm.0.000032.
   PubMed Web of Science ®Google Scholar
• Rabin N, Zheng Y, Opoku-Temeng C, Du Y, Bonsu E, Sintim HO. Biofilm formation mechanisms and targets for developing antibiofilm agents. Future Med Chem. 2015;7(4):493–512. doi:10.4155/fmc.15.6.
   PubMed Web of Science ®Google Scholar
• MacKenzie KD, Palmer MB, Köster WL, White AP. Examining the link between biofilm formation and the ability of pathogenic Salmonella strains to colonize multiple host species. Front Vet Sci. 2017;4: doi:10.3389/fvets.2017.00138.
   PubMed Web of Science ®Google Scholar
• Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 2016;14(9):563–575. doi:https://doi.org/10.1038/nrmicro.2016.94.
   PubMed Web of Science ®Google Scholar
• Lowe JA. Chapter 13. Mechanisms of antibiotic resistance. 1982. p. 119–127. doi:10.1016/S0065-7743(08)60495-9.
   Google Scholar
• Poole K. Bacterial stress responses as determinants of antimicrobial resistance. J Antimicrob Chemother. 2012;67(9):2069–2089. doi:10.1093/jac/dks196.
   PubMed Web of Science ®Google Scholar
• Stewart PS. Diffusion in biofilms. J Bacteriol. 2003;185(5):1485–1491. doi:10.1128/JB.185.5.1485-1491.2003.
   PubMed Web of Science ®Google Scholar
• Behbahani SB, Kiridena SD, Wijayaratna UN, Taylor C, Anker JN, Tzeng TRJ. pH variation in medical implant biofilms: causes, measurements, and its implications for antibiotic resistance. Front Microbiol. 2022;13. doi:10.3389/fmicb.2022.1028560.
   PubMedGoogle Scholar
• Stewart PS. Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol. 2002;292(2):107–113. doi:10.1078/1438-4221-00196.
   PubMed Web of Science ®Google Scholar
• Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol. 2001;39(6):1452–1463. doi:10.1046/j.1365-2958.2001.02337.x.
   PubMed Web of Science ®Google Scholar
• Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SCJ. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res Int. 2012;45(2):502–531. doi:10.1016/j.foodres.2011.01.038.
   Web of Science ®Google Scholar
• Adcox HE, Vasicek EM, Dwivedi V, Hoang KV, Turner J, Gunn JS. Salmonella extracellular matrix components influence biofilm formation and gallbladder colonization. Infect Immun. 2016;84(11):3243–3251. doi:10.1128/IAI.00532-16.
   PubMed Web of Science ®Google Scholar
• Zogaj X, Bokranz W, Nimtz M, Römling U. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect Immun. 2003;71(7):4151–4158. doi:10.1128/IAI.71.7.4151-4158.2003.
   PubMed Web of Science ®Google Scholar
• Hahn MM, González JF, Gunn JS. Salmonella biofilms tolerate hydrogen peroxide by a combination of extracellular polymeric substance barrier function and catalase enzymes. Front Cell Infect Microbiol. 2021;11. doi:10.3389/fcimb.2021.683081.
   PubMed Web of Science ®Google Scholar
• Gibson DL, White AP, Snyder SD, Martin S, Heiss C, Azadi P, Surette M, Kay WW. Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J Bacteriol. 2006;188(22):7722–7730. doi:10.1128/JB.00809-06.
   PubMed Web of Science ®Google Scholar
• Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med. 2012;2(11):a012427–a012427. doi:10.1101/cshperspect.a012427.
   PubMed Web of Science ®Google Scholar
• Janssens JCA, Metzger K, Daniels R, Ptacek D, Verhoeven T, Habel LW, Vanderleyden J, De Vos DE, De Keersmaecker SCJ. Synthesis of N-acyl homoserine lactone analogues reveals strong activators of SdiA, the Salmonella enterica serovar typhimurium LuxR homologue. Appl Environ Microbiol. 2007;73(2):535–544. doi:10.1128/AEM.01451-06.
   PubMed Web of Science ®Google Scholar
• 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. Infect Immun. 2007;75(10):4885–4890. doi:10.1128/IAI.01942-06.
   PubMed Web of Science ®Google Scholar
• Breijyeh Z, Jubeh B, Karaman R. Resistance of gram-negative bacteria to current antibacterial agents and approaches to resolve it. Molecules. 2020;25(6):1340. doi:10.3390/molecules25061340.
   PubMed Web of Science ®Google Scholar
• Ying YC, Bian HS, Tan TMC, Mattmann ME, Geske GD, Igarashi J, Hatano T, Suga H, Blackwell HE, Chua KL, et al. Control of quorum sensing by a Burkholderia pseudomallei multidrug efflux pump. J Bacteriol. 2007;189(11):4320–4324. doi:10.1128/JB.00003-07.
   PubMed Web of Science ®Google Scholar
• Buckley AM, Webber MA, Cooles S, Randall LP, La Ragione RM, Woodward MJ, Piddock LJV. The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell Microbiol. 2006;8(5):847–856. doi:10.1111/j.1462-5822.2005.00671.x.
   PubMed Web of Science ®Google Scholar
• Nishino K, Nikaido E, Yamaguchi A. Regulation and physiological function of multidrug efflux pumps in Escherichia coli and Salmonella. Biochim Biophys Acta Proteins Proteomics. 2009;1794(5):834–843. doi:10.1016/j.bbapap.2009.02.002.
   Web of Science ®Google Scholar
• Martins M, McCusker M, Amaral L, Fanning S. Mechanisms of antibiotic resistance in Salmonella: efflux pumps, genetics, quorum sensing and biofilm formation. Lett Drug Des Discov. 2011;8(2):114–123. doi:10.2174/157018011794183770.
   Web of Science ®Google Scholar
• Fauvart M, de Groote VN, Michiels J. Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J Med Microbiol. 2011;60(6):699–709. doi:10.1099/jmm.0.030932-0.
   PubMed Web of Science ®Google Scholar
• Tezel BU, Akçelik N, Yüksel FN, Karatuğ NT, Akçelik M. Effects of sub-MIC antibiotic concentrations on biofilm production of Salmonella Infantis. Biotechnol Biotechnol Equip. 2016;30(6):1184–1191. doi:10.1080/13102818.2016.1224981.
   Web of Science ®Google Scholar
• Narasanna R. Influence of subinhibitory-concentration (sub-MIC) Cefetoxime on biofilm formation. SEM study of ESBL-producing Salmonella typhi. J Microbiol Infect Dis. 2017;7(2):67–74. doi:10.5799/jmid.328786.
   Google Scholar
• Majtán J, Majtánová Ľ, Xu M, Majtán V. In vitro effect of subinhibitory concentrations of antibiotics on biofilm formation by clinical strains of Salmonella enterica serovar Typhimurium isolated in Slovakia. J Appl Microbiol. 2008;104(5):1294–1301. doi:10.1111/j.1365-2672.2007.03653.x.
   PubMed Web of Science ®Google Scholar
• Koutsolioutsou A, Martins EA, White DG, Levy SB, Demple B. A soxRS-constitutive mutation contributing to antibiotic resistance in a clinical isolate of Salmonella enterica (Serovar typhimurium). Antimicrob Agents Chemother. 2001;45(1):38–43. doi:10.1128/AAC.45.1.38-43.2001.
   PubMed Web of Science ®Google Scholar
• O’Regan E, Quinn T, Pagès J-M, McCusker M, Piddock L, Fanning S. Multiple regulatory pathways associated with high-level ciprofloxacin and multidrug resistance in Salmonella enterica serovar eNteritidis: involvement of ramA and other global regulators. Antimicrob Agents Chemother. 2009;53(3):1080–1087. doi:10.1128/AAC.01005-08.
   PubMed Web of Science ®Google Scholar
• Nonaka L, Maruyama F, Miyamoto M, Miyakoshi M, Kurokawa K, Masuda M. Novel conjugative transferable multiple drug resistance plasmid pAQU1 from Photobacterium damselae subsp. damselae isolated from marine aquaculture environment. Microb Environ. 2012;27(3):263–272. doi:10.1264/jsme2.ME11338.
   PubMed Web of Science ®Google Scholar
• Sugimoto Y, Suzuki S, Nonaka L, Boonla C, Sukpanyatham N, Chou HY, Wu JH. The novel mef(C)–mph(G) macrolide resistance genes are conveyed in the environment on various vectors. J Glob Antimicrob Resist. 2017;10:47–53. doi:10.1016/j.jgar.2017.03.015.
   PubMed Web of Science ®Google Scholar
• Yaron S, Kolling GL, Simon L, Matthews KR. Vesicle-mediated transfer of virulence genes from Escherichia coli O157: h7 to other enteric bacteria. Appl Environ Microbiol. 2000;66(10):4414–4420. doi:10.1128/AEM.66.10.4414-4420.2000.
   PubMed Web of Science ®Google Scholar
• Bai X, Nakatsu CH, Bhunia AK. Bacterial biofilms and their implications in pathogenesis and food safety. Foods. 2021;10(9):2117. doi:10.3390/foods10092117.
   PubMed Web of Science ®Google Scholar
• Gunn JS, Marshall JM, Baker S, Dongol S, Charles RC, Ryan ET. Salmonella chronic carriage: epidemiology, diagnosis, and gallbladder persistence. Trends Microbiol. 2014;22(11):648–655. doi:https://doi.org/10.1016/j.tim.2014.06.007.
   PubMed Web of Science ®Google Scholar
• Schembri MA, Kjærgaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Mol Microbiol. 2003;48(1):253–267. doi:10.1046/j.1365-2958.2003.03432.x.
   PubMed Web of Science ®Google Scholar
• Wang H, Zhang X, Dong Y, Xu X, Zhou G. Insights into the transcriptome profile of mature biofilm of Salmonella Typhimurium on stainless steels surface. Food Res Int. 2015;77:378–384. doi:10.1016/j.foodres.2015.08.034.
   Web of Science ®Google Scholar
• Ghosh S, Lahiri D, Nag M, Sarkar T, Pati S, Edinur HA, Kumar M, Mohd Zain MRA, Ray RR. Precision targeting of food biofilm-forming genes by microbial scissors: cRISPR-Cas as an effective modulator. Front Microbiol. 2022;13: doi:10.3389/fmicb.2022.964848.
   Web of Science ®Google Scholar
• Steenackers HP, Parijs I, Foster KR, Vanderleyden J, Banin E. Experimental evolution in biofilm populations. FEMS Microbiol Rev. 2016;40(3):373–397. doi:10.1093/femsre/fuw002.
   PubMed Web of Science ®Google Scholar
• Coenye T, Bové M, Bjarnsholt T. Biofilm antimicrobial susceptibility through an experimental evolutionary lens. NPJ Biofilms Microbiomes. 2022;8(1):82. doi:10.1038/s41522-022-00346-4.
   PubMed Web of Science ®Google Scholar
• Fuentes-Hernández A, Hernández-Koutoucheva A, Muñoz AF, Palestino RD, Peña-Miller R. Diffusion-driven enhancement of the antibiotic resistance selection window. J R Soc Interface. 2019;16(158):20190363. doi:10.1098/rsif.2019.0363.
   PubMed Web of Science ®Google Scholar
• Hegreness M, Shoresh N, Damian D, Hartl D, Kishony R. Accelerated evolution of resistance in multidrug environments. Proc Natl Acad Sci USA. 2008;105(37):13977–13981. doi:10.1073/pnas.0805965105.
   PubMed Web of Science ®Google Scholar
• Santos-Lopez A, Marshall CW, Scribner MR, Snyder DJ, Cooper VS. Evolutionary pathways to antibiotic resistance are dependent upon environmental structure and bacterial lifestyle. Elife. 2019;8. doi:10.7554/eLife.47612.
   PubMed Web of Science ®Google Scholar
• Ahmed MN, Porse A, Sommer MOA, Høiby N, Ciofu O. Evolution of antibiotic resistance in biofilm and planktonic pseudomonas aeruginosa populations exposed to subinhibitory levels of ciprofloxacin. Antimicrob Agents Chemother. 2018;62(8). doi:10.1128/AAC.00320-18.
   Web of Science ®Google Scholar
• Ahmed MN, Abdelsamad A, Wassermann T, Porse A, Becker J, Sommer MOA, Høiby N, Ciofu O. The evolutionary trajectories of P. aeruginosa in biofilm and planktonic growth modes exposed to ciprofloxacin: beyond selection of antibiotic resistance. NPJ Biofilms Microbiomes. 2020;6(1). doi:10.1038/s41522-020-00138-8.
   PubMed Web of Science ®Google Scholar
• MacKenzie KD, Wang Y, Shivak DJ, Wong CS, Hoffman LJL, Lam S, Kröger C, Cameron ADS, Townsend HGG, Köster W, et al. Bistable expression of CsgD in Salmonella enterica serovar typhimurium connects virulence to persistence. Infect Immun. 2015;83(6):2312–2326. doi:10.1128/IAI.00137-15.
   PubMed Web of Science ®Google Scholar
• Lories B, Roberfroid S, Dieltjens L, De Coster D, Foster KR, Steenackers HP. Biofilm bacteria use stress responses to detect and respond to competitors. Curr Biol. 2020;30(7):1231–1244.e4. doi:10.1016/j.cub.2020.01.065.
   PubMed Web of Science ®Google Scholar
• Zou Y, Woo J, Ahn J. Cellular and molecular responses of Salmonella Typhimurium to antimicrobial-induced stresses during the planktonic-to-biofilm transition. Lett Appl Microbiol. 2012;55(4):274–282. doi:10.1111/j.1472-765X.2012.03288.x.
   PubMed Web of Science ®Google Scholar
• Chin KCJ, Taylor TD, Hebrard M, Anbalagan K, Dashti MG, Phua KK. Transcriptomic study of Salmonella enterica subspecies enterica serovar Typhi biofilm. Bmc Genom. 2017;18(1). doi:10.1186/s12864-017-4212-6.
   Google Scholar
• Orme R, Douglas CWI, Rimmer S, Webb M. Proteomic analysis of Escherichia coli biofilms reveals the overexpression of the outer membrane protein OmpA. Proteomics. 2006;6(15):4269–4277. doi:10.1002/pmic.200600193.
   PubMed Web of Science ®Google Scholar
• Hamilton S, Bongaerts RJ, Mulholland F, Cochrane B, Porter J, Lucchini S, Lappin-Scott HM, Hinton JC. The transcriptional programme of Salmonella enterica serovar Typhimurium reveals a key role for tryptophan metabolism in biofilms. Bmc Genom. 2009;10(1). doi:10.1186/1471-2164-10-599.
   PubMedGoogle Scholar
• Tabak M, Scher K, Hartog E, Romling U, Matthews KR, Chikindas ML, Yaron S. Effect of triclosan on Salmonella typhimurium at different growth stages and in biofilms. FEMS Microbiol Lett. 2007;267(2):200–206. doi:10.1111/j.1574-6968.2006.00547.x.
   PubMed Web of Science ®Google Scholar
• Barbosa TM, Levy SB. Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA. J Bacteriol. 2000;182(12):3467–3474. doi:10.1128/JB.182.12.3467-3474.2000.
   PubMed Web of Science ®Google Scholar
• Pasqua M, Grossi M, Zennaro A, Fanelli G, Micheli G, Barras F, Colonna B, Prosseda G. The varied role of efflux pumps of the mfs family in the interplay of bacteria with animal and plant cells. Microorganisms. 2019;7(9):285. doi:10.3390/microorganisms7090285.
   PubMed Web of Science ®Google Scholar
• Yamasaki S, Nagasawa S, Fukushima A, Hayashi-Nishino M, Nishino K. Cooperation of the multidrug efflux pump and lipopolysaccharides in the intrinsic antibiotic resistance of Salmonella enterica serovar Typhimurium. J Antimicrob Chemother. 2013;68(5):1066–1070. doi:10.1093/jac/dks528.
   PubMed Web of Science ®Google Scholar
• Nishino K, Latifi T, Groisman EA. Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol Microbiol. 2006;59(1):126–141. doi:10.1111/j.1365-2958.2005.04940.x.
   PubMed Web of Science ®Google Scholar
• Baugh S, Ekanayaka AS, Piddock LJV, Webber MA. Loss of or inhibition of all multidrug resistance efflux pumps of Salmonella enterica serovar Typhimurium results in impaired ability to form a biofilm. J Antimicrob Chemother. 2012;67(10):2409–2417. doi:10.1093/jac/dks228.
   PubMed Web of Science ®Google Scholar
• Andersen JL, He G-X, Kakarla P, Kc R, Kumar S, Lakra W, Mukherjee M, Ranaweera I, Shrestha U, Tran T, et al. Multidrug efflux pumps from Enterobacteriaceae, Vibrio cholerae and Staphylococcus aureus bacterial food pathogens. Int J Env Res Pub He. 2015;12(2):1487–1547. doi:10.3390/ijerph120201487.
   PubMed Web of Science ®Google Scholar
• Kapach G, Nuri R, Schmidt C, Danin A, Ferrera S, Savidor A, Gerlach RG, Shai Y. Loss of the periplasmic chaperone skp and mutations in the efflux pump AcrAB-TolC play a role in acquired resistance to antimicrobial peptides in Salmonella typhimurium. Front Microbiol. 2020;11. doi:10.3389/fmicb.2020.00189.
   PubMed Web of Science ®Google Scholar
• Hayashi M, Tabata K, Yagasaki M, Yonetani Y. Effect of multidrug-efflux transporter genes on dipeptide resistance and overproduction in Escherichia coli. FEMS Microbiol Lett. 2010;304(1):12–19. doi:10.1111/j.1574-6968.2009.01879.x.
   PubMed Web of Science ®Google Scholar
• Hancock V, Klemm P. Global gene expression profiling of asymptomatic bacteriuria Escherichia coli during biofilm growth in human urine. Infect Immun. 2007;75(2):966–976. doi:10.1128/IAI.01748-06.
   PubMed Web of Science ®Google Scholar
• Nishino K, Yamaguchi A. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol. 2001;183(20):5803–5812. doi:10.1128/JB.183.20.5803-5812.2001.
   PubMed Web of Science ®Google Scholar
• Boyd D, Peters GA, Cloeckaert A, Boumedine KS, Chaslus-Dancla E, Imberechts H, Mulvey MR. Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar typhimurium DT104 and its identification in phage type DT120 and serovar agona. J Bacteriol. 2001;183(19):5725–5732. doi:10.1128/JB.183.19.5725-5732.2001.
   PubMed Web of Science ®Google Scholar
• Villagra NA, Fuentes JA, Jofre MR, Hidalgo AA, Garcia P, Mora GC. The carbon source influences the efflux pump-mediated antimicrobial resistance in clinically important Gram-negative bacteria. J Antimicrob Chemother. 2012;67(4):921–927. doi:10.1093/jac/dkr573.
   PubMed Web of Science ®Google Scholar
• Marsh D, Henderson PJF. Specific spin labelling of the sugar-H+ symporter, GalP, in cell membranes of Escherichia coli: site mobility and overall rotational diffusion of the protein. Biochim Biophys Acta Biomembr. 2001;1510(1–2):464–473. doi:10.1016/S0005-2736(00)00377-1.
   Web of Science ®Google Scholar
• Postma PW. Galactose transport in Salmonella typhimurium. J Bacteriol. 1977;129(2):630–639. doi:10.1128/jb.129.2.630-639.1977.
   PubMed Web of Science ®Google Scholar
• Weston N, Sharma P, Ricci V, Piddock LJV. Regulation of the AcrAB-TolC efflux pump in Enterobacteriaceae. Res Microbiol. 2018;169(7–8):425–431. doi:10.1016/j.resmic.2017.10.005.
   PubMed Web of Science ®Google Scholar
• Du D, Wang Z, James NR, Voss JE, Klimont E, Ohene-Agyei T, Venter H, Chiu W, Luisi BF. Structure of the AcrAB–TolC multidrug efflux pump. Nature. 2014;509(7501):512–515. doi:10.1038/nature13205.
   PubMed Web of Science ®Google Scholar
• Horiyama T, Yamaguchi A, Nishino K. TolC dependency of multidrug efflux systems in Salmonella enterica serovar Typhimurium. J Antimicrob Chemother. 2010;65(7):1372–1376. doi:10.1093/jac/dkq160.
   PubMed Web of Science ®Google Scholar
• Hwang J, Park S-H, Lee CW, Do H, Shin SC, Kim H-W, Lee SG, Park HH, Kwon S, Lee JH, et al. Crystal structure of a MarR family protein from the psychrophilic bacterium Paenisporosarcina sp. TG-14 in complex with a lipid-like molecule. IUCrJ. 2021;8(5):842–852. doi:10.1107/S2052252521005704.
   PubMedGoogle Scholar
• Martin RG, Rosner JL. Genomics of the marA/soxS/rob regulon of Escherichia coli: identification of directly activated promoters by application of molecular genetics and informatics to microarray data. Mol Microbiol. 2002;44(6):1611–1624. doi:10.1046/j.1365-2958.2002.02985.x.
   PubMed Web of Science ®Google Scholar
• Beggs GA, Brennan RG, Arshad M. MarR family proteins are important regulators of clinically relevant antibiotic resistance. Protein Sci. 2020;29(3):647–653. doi:10.1002/pro.3769.
   PubMed Web of Science ®Google Scholar
• Perera IC, Grove A. Molecular mechanisms of ligand-mediated attenuation of DNA binding by MarR family transcriptional regulators. J Mol Cell Biol. 2010;2(5):243–254. doi:10.1093/jmcb/mjq021.
   PubMed Web of Science ®Google Scholar
• Prieto AI, Herández SB, Cota I, Pucciarelli MG, Orlov Y, Ramos-Morales F, García-Del Portillo F, Casadesus J. Roles of the outer membrane protein asmA of Salmonella enterica in the control of marRAB expression and invasion of epithelial cells. J Bacteriol. 2009;191(11):3615–3622. doi:10.1128/JB.01592-08.
   PubMed Web of Science ®Google Scholar
• Feng Z, Liu D, Wang L, Wang Y, Zang Z, Liu Z, Song B, Gu L, Fan Z, Yang S, et al. A putative efflux transporter of the ABC family, YbhFSR, in Escherichia coli functions in tetracycline efflux and Na+(Li+)/H+ Transport. Front Microbiol. 2020;11. doi:10.3389/fmicb.2020.00556.
   Web of Science ®Google Scholar
• Choi U, Lee CR. Distinct roles of outer membrane porins in antibiotic resistance and membrane integrity in Escherichia coli. Front Microbiol. 2019;10. doi:10.3389/fmicb.2019.00953.
   Google Scholar
• Pagès JM, James CE, Winterhalter M. The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. Nat Rev Microbiol. 2008;6(12):893–903. doi:10.1038/nrmicro1994.
   PubMed Web of Science ®Google Scholar
• Moya-Torres A, Mulvey MR, Kumar A, Oresnik IJ, Brassinga AKC. The lack of OmpF, but not OmpC, contributes to increased antibiotic resistance in Serratia marcescens. Microbiology (UK). 2014;160(9):1882–1892. doi:10.1099/mic.0.081166-0.
   PubMedGoogle Scholar
• Villarreal JM, Becerra-Lobato N, Rebollar-Flores JE, Medina-Aparicio L, Carbajal-Gómez E, Zavala-García ML, Vázquez A, Gutiérrez-Ríos RM, Olvera L, Encarnación S, et al. The Salmonella enterica serovar Typhi ltrR-ompR-ompC-ompF genes are involved in resistance to the bile salt sodium deoxycholate and in bacterial transformation. Mol Microbiol. 2014;92(5):1005–1024. doi:10.1111/mmi.12610.
   PubMed Web of Science ®Google Scholar
• Shi C, Li M, Muhammad I, Ma X, Chang Y, Li R, Li C, He J, Liu F. Combination of berberine and ciprofloxacin reduces multi-resistant Salmonella strain biofilm formation by depressing mRNA expressions of luxS, rpoE, and ompR. J Vet Sci. 2018;19(6):808. doi:10.4142/jvs.2018.19.6.808.
   PubMed Web of Science ®Google Scholar
• Perni S, Preedy EC, Landini P, Prokopovich P. Influence of csgD and ompR on nanomechanics, adhesion forces, and curli properties of E. coli. Langmuir. 2016;32(31):7965–7974. doi:10.1021/acs.langmuir.6b02342.
   PubMed Web of Science ®Google Scholar
• Ziervogel BK, Roux B. The binding of antibiotics in OmpF porin. Structure. 2013;21(1):76–87. doi:10.1016/j.str.2012.10.014.
   PubMed Web of Science ®Google Scholar
• Matera G, Altuvia Y, Gerovac M, El Mouali Y, Margalit H, Vogel J. Global RNA interactome of Salmonella discovers a 5′ UTR sponge for the MicF small RNA that connects membrane permeability to transport capacity. Mol Cell. 2022;82(3):629–644.e4. doi:10.1016/j.molcel.2021.12.030.
   PubMed Web of Science ®Google Scholar
• Medeiros AA, O’Brien TF, Rosenberg EY, Nikaido H. Loss of OmpC porin in a strain of salmonella typhimirium causes increased resistance to cephalosporins during therapy. J Infect Dis. 1987;156(5):751–757. doi:10.1093/infdis/156.5.751.
   PubMed Web of Science ®Google Scholar
• Chowdhury AR, Mukherjee D, Singh AK, Chakravortty D. Loss of outer membrane protein a (OmpA) impairs the survival of Salmonella Typhimurium by inducing membrane damage in the presence of ceftazidime and meropenem. J Antimicrob Chemother. 2022;77(12):3376–3389. doi:10.1093/jac/dkac327.
   PubMed Web of Science ®Google Scholar
• Smani Y, Fàbrega A, Roca I, Sánchez-Encinales V, Vila J, Pachón J. Role of OmpA in the multidrug resistance phenotype of Acinetobacter baumannii. Antimicrob Agents Chemother. 2014;58(3):1806–1808. doi:10.1128/AAC.02101-13.
   PubMed Web of Science ®Google Scholar
• Dupont M, James CE, Chevalier J, Pagès JM. An early response to environmental stress involves regulation of OmpX and OmpF, two enterobacterial outer membrane pore-forming proteins. Antimicrob Agents Chemother. 2007;51(9):3190–3198. doi:10.1128/AAC.01481-06.
   PubMed Web of Science ®Google Scholar
• Briones AC, Lorca D, Cofre A, Cabezas CE, Krüger GI, Pardo-Esté C, Baquedano MS, Salinas CR, Espinoza M, Castro-Severyn J, et al. Genetic regulation of the ompX porin of Salmonella Typhimurium in response to hydrogen peroxide stress. Biol Res. 2022;55(1). doi:10.1186/s40659-022-00377-3.
   PubMed Web of Science ®Google Scholar
• Hirakawa H, Suzue K, Takita A, Kamitani W, Tomita H, Brodsky IE. Roles of ompx, an outer membrane protein, on virulence and flagellar expression in uropathogenic Escherichia coli. Infect Immun. 2021;89(6). doi:10.1128/IAI.00721-20.
   PubMed Web of Science ®Google Scholar
• Wang Y, Yi L, Zhang J, Sun L, Wen W, Zhang C, Wang S. Functional analysis of superoxide dismutase of Salmonella typhimurium in serum resistance and biofilm formation. J Appl Microbiol. 2018;125(5):1526–1533. doi:10.1111/jam.14044.
   PubMed Web of Science ®Google Scholar
• Stevanin TM, Poole RK, Demoncheaux EAG, Read RC. Flavohemoglobin Hmp protects Salmonella enterica serovar typhimurium from nitric oxide-related killing by human macrophages. Infect Immun. 2002;70(8):4399–4405. doi:10.1128/IAI.70.8.4399-4405.2002.
   PubMed Web of Science ®Google Scholar
• Fukuda M, Takeda H, Kato HE, Doki S, Ito K, Maturana AD, Ishitani R, Nureki O. Structural basis for dynamic mechanism of nitrate/nitrite antiport by NarK. Nat Commun. 2015;6(1). doi:10.1038/ncomms8097.
   Google Scholar
• Jia W, Tovell N, Clegg S, Trimmer M, Cole J. A single channel for nitrate uptake, nitrite export and nitrite uptake by Escherichia coli NarU and a role for NirC in nitrite export and uptake. Biochem J. 2009;417(1):297–307. doi:10.1042/BJ20080746.
   PubMedGoogle Scholar
• Wand ME, Bock LJ, Bonney LC, Sutton JM. Mechanisms of increased resistance to chlorhexidine and cross-resistance to colistin following exposure of Klebsiella pneumoniae clinical isolates to chlorhexidine. Antimicrob Agents Chemother. 2017;61(1). doi:10.1128/AAC.01162-16.
   PubMed Web of Science ®Google Scholar
• Sakai A, Nakanishi M, Yoshiyama K, Maki H. Impact of reactive oxygen species on spontaneous mutagenesis in Escherichia coli. Genes to Cells. 2006;11(7):767–778. doi:10.1111/j.1365-2443.2006.00982.x.
   PubMed Web of Science ®Google Scholar
• Cosgrove K, Coutts G, Jonsson I-M, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ. Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol. 2007;189(3):1025–1035. doi:10.1128/JB.01524-06.
   PubMed Web of Science ®Google Scholar
• Jacobson FS, Morgan RW, Christman MF, Ames BN. An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. J Biol Chem. 1989;264(3):1488–1496. doi:10.1016/S0021-9258(18)94214-6.
   PubMed Web of Science ®Google Scholar
• Parsonage D, Karplus PA, Poole LB. Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. Proc Natl Acad Sci USA. 2008;105(24):8209–8214. doi:10.1073/pnas.0708308105.
   PubMed Web of Science ®Google Scholar
• Bollinger N, Hassett DJ, Iglewski BH, Costerton JW, McDermott TR. Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J Bacteriol. 2001;183(6):1990–1996. doi:10.1128/JB.183.6.1990-1996.2001.
   PubMed Web of Science ®Google Scholar
• Jang IA, Kim J, Park W. Endogenous hydrogen peroxide increases biofilm formation by inducing exopolysaccharide production in Acinetobacter oleivorans DR1. Sci Rep. 2016;6(1). doi:10.1038/srep21121.
   Google Scholar
• Loewen PC, De Silva PM, Donald LJ, Switala J, Villanueva J, Fita I, Kumar A. KatG-Mediated oxidation leading to reduced susceptibility of bacteria to kanamycin. ACS Omega. 2018;3(4):4213–4219. doi:10.1021/acsomega.8b00356.
   PubMed Web of Science ®Google Scholar
• Zhu Y-Q, Zhu D-Y, Lu H-X, Yang N, Li G-P, Wang D-C. Purification and preliminary crystallographic studies of CutC, a novel copper homeostasis protein from shigella flexneri. Protein Pept Lett. 2005;12(8):823–826. doi:10.2174/0929866054864184.
   PubMed Web of Science ®Google Scholar
• Grass G, Rensing C, Solioz M. Metallic copper as an antimicrobial surface. Appl Environ Microb. 2011;77(5):1541–1547. doi:10.1128/AEM.02766-10.
   PubMed Web of Science ®Google Scholar
• Gupta SD, Lee BTO, Camakaris J, Wu HC. Identification of cutC and cutF (nlpE) genes involved in copper tolerance in Escherichia coli. J Bacteriol. 1995;177(15):4207–4215. doi:10.1128/jb.177.15.4207-4215.1995.
   PubMed Web of Science ®Google Scholar
• Geslin C, Llanos J, Prieur D, Jeanthon C. The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res Microbiol. 2001;152(10):901–905. doi:10.1016/S0923-2508(01)01273-6.
   PubMed Web of Science ®Google Scholar
• Calhoun LN, Kwon YM. The ferritin-like protein Dps protects Salmonella enterica serotype Enteritidis from the Fenton-mediated killing mechanism of bactericidal antibiotics. Int J Antimicrob Agents. 2011;37(3):261–265. doi:10.1016/j.ijantimicag.2010.11.034.
   PubMed Web of Science ®Google Scholar
• Nair S, Finkel SE. Dps protects cells against multiple stresses during stationary phase. J Bacteriol. 2004;186(13):4192–4198. doi:10.1128/JB.186.13.4192-4198.2004.
   PubMed Web of Science ®Google Scholar
• Almiron M, Link AJ, Furlong D, Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 1992;6(12b):2646–2654. doi:10.1101/gad.6.12b.2646.
   PubMed Web of Science ®Google Scholar
• Goto R, Miki T, Nakamura N, Fujimoto M, Okada N, Cloeckaert A. Salmonella Typhimurium PagP- and UgtL-dependent resistance to antimicrobial peptides contributes to the gut colonization. PLoS One. 2017;12(12):e0190095. doi:10.1371/journal.pone.0190095.
   PubMed Web of Science ®Google Scholar
• Shi Y, Cromie MJ, Hsu FF, Turk J, Groisman EA. PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B. Mol Microbiol. 2004;53(1):229–241. doi:10.1111/j.1365-2958.2004.04107.x.
   PubMed Web of Science ®Google Scholar
• Pardo-Esté C, Castro-Severyn J, Krüger GI, Cabezas CE, Briones AC, Aguirre C, Morales N, Baquedano MS, Sulbaran YN, Hidalgo AA, et al. The transcription factor ArcA Modulates Salmonella’s metabolism in response to neutrophil hypochlorous acid-mediated stress. Front Microbiol. 2019;10. doi:10.3389/fmicb.2019.02754.
   Web of Science ®Google Scholar
• Zhang XS, García-Contreras R, Wood TK. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J Bacteriol. 2007;189(8):3051–3062. doi:10.1128/JB.01832-06.
   PubMed Web of Science ®Google Scholar
• Salazar JK, Deng K, Tortorello ML, Brandl MT, Wang H, Zhang W. Genes ycfR, sirA and yigG contribute to the surface attachment of Salmonella enterica typhimurium and saintpaul to fresh produce. PLoS One. 2013;8(2):e57272. doi:10.1371/journal.pone.0057272.
   PubMed Web of Science ®Google Scholar
• Nobre LS, Al-Shahrour F, Dopazo J, Saraiva LM. Exploring the antimicrobial action of a carbon monoxide-releasing compound through whole-genome transcription profiling of Escherichia coli. Microbiology (NY). 2009;155:813–824.
   PubMed Web of Science ®Google Scholar
• Conter A, Gangneux C, Suzanne M, Gutierrez C. Survival of Escherichia coli during long-term starvation: effects of aeration, NaCl, and the rpoS and osmC gene products. Res Microbiol. 2001;152(1):17–26. doi:10.1016/S0923-2508(00)01164-5.
   PubMed Web of Science ®Google Scholar
• Mongkolsuk S, Praituan W, Loprasert S, Fuangthong M, Chamnongpol S. Identification and characterization of a new organic hydroperoxide resistance (ohr) gene with a novel pattern of oxidative stress regulation from Xanthomonas campestris pv. phaseoli. J Bacteriol. 1998;180(10):2636–2643. doi:10.1128/JB.180.10.2636-2643.1998.
   PubMed Web of Science ®Google Scholar
• Vickery K. Special Issue: microbial biofilms in healthcare: formation, prevention and treatment. Materials. 2019;12(12):2001. doi:10.3390/ma12122001.
   PubMed Web of Science ®Google Scholar
• Schulze A, Mitterer F, Pombo JP, Schild S. Biofilms by bacterial human pathogens: clinical relevance - Development, composition and regulation - Therapeutical strategies. Microb Cell. 2021;8(2):28–56. doi:10.15698/mic2021.02.741.
   PubMed Web of Science ®Google Scholar
• Madsen JS, Burmølle M, Hansen LH, Sørensen SJ. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Microbiol. 2012;65(2):183–195. doi:10.1111/j.1574-695X.2012.00960.x.
   PubMedGoogle Scholar
• Gamazo C, Solano C, Lasa I. Biofilm formation by Salmonella in food processing environments. In: Biofilms in the food and beverage industries. Elsevier; 2009. pp. 226–249. doi:10.1533/9781845697167.2.226
   Google Scholar
• Joseph B, Otta SK, Karunasagar I, Karunasagar I. Biofilm formation by Salmonella spp. On food contact surfaces and their sensitivity to sanitizers. Int J Food Microbiol. 2001;64(3):367–372. doi:10.1016/S0168-1605(00)00466-9.
   PubMed Web of Science ®Google Scholar
• Liu H, Whitehouse CA, Li B. Presence and persistence of Salmonella in water: the impact on microbial quality of water and food safety. Front Public Health. 2018;6: doi:10.3389/fpubh.2018.00159.
   Web of Science ®Google Scholar
• Liu Z, Adyel TM, Miao L, You G, Liu S, Hou J. Biofilm influenced metal accumulation onto plastic debris in different freshwaters. Environ Pollut. 2021;285:117646. doi:10.1016/j.envpol.2021.117646.
   PubMed Web of Science ®Google Scholar
• Cloete TE, Jacobs L, Brözel VS. The chemical control of biofouling in industrial water systems. Biodegradation. 1998;9(1):23–37. doi:10.1023/A:1008216209206.
   PubMed Web of Science ®Google Scholar
• Colclough A, Corander J, Sheppard SK, Bayliss SC, Vos M. Patterns of cross-resistance and collateral sensitivity between clinical antibiotics and natural antimicrobials. Evol Appl. 2019;12(5):878–887. doi:10.1111/eva.12762.
   PubMed Web of Science ®Google Scholar
• Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence. 2018;9(1):522–554. doi:10.1080/21505594.2017.1313372.
   PubMed Web of Science ®Google Scholar
• Pogodin S, Hasan J, Baulin V, Webb H, Truong V, Phong Nguyen T, Boshkovikj V, Fluke C, Watson G, Watson J, et al. Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys J. 2013;104(4):835–840. doi:10.1016/j.bpj.2012.12.046.
   PubMed Web of Science ®Google Scholar
• Banat IM, De Rienzo MAD, Quinn GA. Microbial biofilms: biosurfactants as antibiofilm agents. Appl Microbiol Biotechnol. 2014;98(24):9915–9929. doi:10.1007/s00253-014-6169-6.
   PubMed Web of Science ®Google Scholar
• Brackman G, Coenye T. Quorum sensing inhibitors as anti-biofilm agents. Curr Pharm Des. 2014;21(1):5–11. doi:10.2174/1381612820666140905114627.
   Web of Science ®Google Scholar
• Ren D, Sims JJ, Wood TK. Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3- butyl-2(5H)-furanone. Environ Microbiol. 2001;3(11):731–736. doi:10.1046/j.1462-2920.2001.00249.x.
   PubMed Web of Science ®Google Scholar
• Li X-H, Lee J-H. Antibiofilm agents: a new perspective for antimicrobial strategy. J Microbiol. 2017;55(10):753–766. doi:10.1007/s12275-017-7274-x.
   PubMed Web of Science ®Google Scholar