The role of chemotaxis and efflux pumps on nitrate reduction in the toxic regions of a ciprofloxacin concentration gradient
1.DeVries SL, Zhang P. Antibiotics and the Terrestrial Nitrogen Cycle: a review. Curr Pollut Rep. 2016;2:51–67.CAS
Article
Google Scholar
2.Kümmerer K. Antibiotics in the aquatic environment – A review – Part I. Chemosphere. 2009;75:417–34.PubMed
PubMed Central
Article
CAS
Google Scholar
3.Franklin AM, Aga DS, Cytryn E, Durso LM, McLain JE, Pruden A, et al. Antibiotics in Agroecosystems: introduction to the Special Section. J Environ Qual. 2016;45:377–93.CAS
PubMed
Article
PubMed Central
Google Scholar
4.Roose-Amsaleg C, Laverman AM. Do antibiotics have environmental side-effects? Impact of synthetic antibiotics on biogeochemical processes. Environ Sci Pollut Res. 2016;23:4000–12.CAS
Article
Google Scholar
5.Grenni P, Ancona V, Barra, Caracciolo A. Ecological effects of antibiotics on natural ecosystems: a review. Microchemical J. 2018;136:25–39.CAS
Article
Google Scholar
6.Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin Y-F, Yannarell AC, et al. Fate and Transport of Antibiotic Residues and Antibiotic Resistance Genes following Land Application of Manure Waste. J Environ Qual. 2009;38:1086.CAS
PubMed
Article
PubMed Central
Google Scholar
7.Mehrtens A, Licha T, Broers HP, Burke V. Tracing veterinary antibiotics in the subsurface – A long-term field experiment with spiked manure. Environ Pollut. 2020;265:114930.CAS
PubMed
Article
PubMed Central
Google Scholar
8.Kivits T, Broers HP, Beeltje H, van Vliet M, Griffioen J. Presence and fate of veterinary antibiotics in age-dated groundwater in areas with intensive livestock farming. Environ Pollut. 2018;241:988–98.CAS
PubMed
Article
PubMed Central
Google Scholar
9.Gros M, Mas-Pla J, Boy-Roura M, Geli I, Domingo F, Petrović M. Veterinary pharmaceuticals and antibiotics in manure and slurry and their fate in amended agricultural soils: Findings from an experimental field site (Baix Empordà, NE Catalonia). Sci Total Environ. 2019;654:1337–49.CAS
PubMed
Article
PubMed Central
Google Scholar
10.Baquero F, Negri M-C. Challenges: selective compartments for resistant microorganisms in antibiotic gradients. BioEssays. 1997;19:731–6.CAS
PubMed
PubMed Central
Article
Google Scholar
11.Hermsen R, Deris JB, Hwa T. On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient. Proc Natl Acad Sci. 2012;109:10775–80.CAS
PubMed
Article
PubMed Central
Google Scholar
12.Andersson DI, Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol. 2014;12:465–78.CAS
PubMed
Article
PubMed Central
Google Scholar
13.Levin-Reisman I, Ronin I, Gefen O, Braniss I, Shoresh N, Balaban NQ. Antibiotic tolerance facilitates the evolution of resistance. Science. 2017;355:826–30.CAS
PubMed
Article
PubMed Central
Google Scholar
14.Cohen NR, Lobritz MA, Collins JJ. Microbial Persistence and the Road to Drug Resistance. Cell Host Microbe. 2013;13:632–42.CAS
PubMed
PubMed Central
Article
Google Scholar
15.Hughes D, Andersson DI. Environmental and genetic modulation of the phenotypic expression of antibiotic resistance. FEMS Microbiol Rev. 2017;41:374–91.CAS
PubMed
PubMed Central
Article
Google Scholar
16.Venter H, Arzanlou M, Chai WC, Venter H. Intrinsic, adaptive and acquired antimicrobial resistance in Gram-negative bacteria. Essays Biochem. 2017;61:49–59.PubMed
Article
PubMed Central
Google Scholar
17.Alcalde RE, Michelson K, Zhou L, Schmitz EV, Deng J, Sanford RA, et al. Motility of Shewanella oneidensis MR-1 Allows for Nitrate Reduction in the Toxic Region of a Ciprofloxacin Concentration Gradient in a Microfluidic Reactor. Environ Sci Technol. 2019;53:2778–87.CAS
PubMed
Article
PubMed Central
Google Scholar
18.Hol FJH, Hubert B, Dekker C, Keymer JE. Density-dependent adaptive resistance allows swimming bacteria to colonize an antibiotic gradient. ISME J. 2016;10:30–38.CAS
PubMed
Article
PubMed Central
Google Scholar
19.Butler MT, Wang Q, Harshey RM. Cell density and mobility protect swarming bacteria against antibiotics. Proc Natl Acad Sci. 2010;107:3776–81.CAS
PubMed
Article
PubMed Central
Google Scholar
20.Steel H, Papachristodoulou A. The effect of spatiotemporal antibiotic inhomogeneities on the evolution of resistance. J Theor Biol. 2020;486:110077.PubMed
Article
PubMed Central
Google Scholar
21.Lai S, Tremblay J, Déziel E. Swarming motility: a multicellular behaviour conferring antimicrobial resistance. Environ Microbiol. 2009;11:126–36.CAS
PubMed
Article
PubMed Central
Google Scholar
22.Zhang Q, Lambert G, Liao D, Kim H, Robin K, Tung C-k, et al. Acceleration of Emergence of Bacterial Antibiotic Resistance in Connected Microenvironments. Science. 2011;333:1764–7.CAS
PubMed
Article
PubMed Central
Google Scholar
23.Wu A, Loutherback K, Lambert G, Estevez-Salmeron L, Tlsty TD, Austin RH, et al. Cell motility and drug gradients in the emergence of resistance to chemotherapy. Proc Natl Acad Sci. 2013;110:16103–8.CAS
PubMed
Article
PubMed Central
Google Scholar
24.Baym M, Lieberman TD, Kelsic ED, Chait R, Gross R, Yelin I, et al. Spatiotemporal microbial evolution on antibiotic landscapes. Science. 2016;353:1147–51.CAS
PubMed
PubMed Central
Article
Google Scholar
25.Alexandre G, Greer-Phillips S, Zhulin IB. Ecological role of energy taxis in microorganisms. FEMS Microbiol Rev. 2004;28:113–26.CAS
PubMed
Article
PubMed Central
Google Scholar
26.Fenchel T. Microbial Behavior in a Heterogeneous World. Science. 2002;296:1068–71.CAS
PubMed
Article
PubMed Central
Google Scholar
27.Groh JL, Luo Q, Ballard JD, Krumholz LR. Genes That Enhance the Ecological Fitness of Shewanella oneidensis MR-1 in Sediments Reveal the Value of Antibiotic Resistance. Appl Environ Microbiol. 2007;73:492–8.CAS
PubMed
Article
PubMed Central
Google Scholar
28.Blair JM, Piddock LJ. Structure, function and inhibition of RND efflux pumps in Gram-negative bacteria: an update. Curr Opin Microbiol. 2009;12:512–9.CAS
PubMed
Article
PubMed Central
Google Scholar
29.Fernández L, Hancock REW. Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance. Clin Microbiol Rev. 2012;25:661–81.PubMed
PubMed Central
Article
CAS
Google Scholar
30.Alvarez-Ortega C, Olivares J, Martinez JL. RND multidrug efflux pumps: what are they good for? Front Microbiol. 2013;4:7.PubMed
PubMed Central
Article
Google Scholar
31.Anes J, McCusker MP, Fanning S, Martins M. The ins and outs of RND efflux pumps in Escherichia coli. Front Microbiol. 2015;6:587.PubMed
PubMed Central
Article
Google Scholar
32.Ma D, Alberti M, Lynch C, Nikaido H, Hearst JE. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol Microbiol. 1996;19:101–12.CAS
PubMed
Article
PubMed Central
Google Scholar
33.Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev. 2003;27:313–39.CAS
PubMed
Article
PubMed Central
Google Scholar
34.Fraud S, Poole K. Oxidative Stress Induction of the MexXY Multidrug Efflux Genes and Promotion of Aminoglycoside Resistance Development in Pseudomonas aeruginosa. Antimicrobial Agents Chemother. 2011;55:1068–74.CAS
Article
Google Scholar
35.El Garch F, Lismond A, Piddock LJV, Courvalin P, Tulkens PM, Van Bambeke F. Fluoroquinolones induce the expression of patA and patB, which encode ABC efflux pumps in Streptococcus pneumoniae. J Antimicrob Chemother. 2010;65:2076–82.CAS
PubMed
Article
PubMed Central
Google Scholar
36.Zhang L, Mah T-F. Involvement of a Novel Efflux System in Biofilm-Specific Resistance to Antibiotics. J Bacteriol. 2008;190:4447–52.CAS
PubMed
PubMed Central
Article
Google Scholar
37.El Meouche I, Siu Y, Dunlop MJ. Stochastic expression of a multiple antibiotic resistance activator confers transient resistance in single cells. Scientific Rep. 2016;6:1–9.Article
CAS
Google Scholar
38.Frade VMF, Dias M, Teixeira ACSC, Palma MSA, Frade VMF, Dias M. et al. Environmental contamination by fluoroquinolones. Braz J Pharm Sci. 2014;50:41–54.Article
Google Scholar
39.Riaz L, Mahmood T, Yang Q, Coyne MS, D’Angelo E. Bacteria-assisted removal of fluoroquinolones from wheat rhizospheres in an agricultural soil. Chemosphere. 2019;226:8–16.CAS
PubMed
Article
Google Scholar
40.Llanes C, Köhler T, Patry I, Dehecq B, Delden C, van, Plésiat P. Role of the MexEF-OprN Efflux System in Low-Level Resistance of Pseudomonas aeruginosa to Ciprofloxacin. Antimicrobial Agents Chemother. 2011;55:5676–84.CAS
Article
Google Scholar
41.Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.CAS
PubMed
PubMed Central
Article
Google Scholar
42.Deatherage DE, Barrick JE. Identification of mutations in laboratory evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol. 2014;1151:165–88.CAS
PubMed
PubMed Central
Article
Google Scholar
43.Saltikov CW, Newman DK. Genetic identification of a respiratory arsenate reductase. PNAS. 2003;100:10983–8.CAS
PubMed
Article
PubMed Central
Google Scholar
44.Engler C, Kandzia R, Marillonnet S. A One Pot, One Step, Precision Cloning Method with High Throughput Capability. PLOS ONE. 2008;3:e3647.PubMed
PubMed Central
Article
CAS
Google Scholar
45.European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin Microbiol Infect. 2003;9:ix–xv.Article
Google Scholar
46.Lambert RJ, Pearson J. Susceptibility testing: accurate and reproducible minimum inhibitory concentration (MIC) and non-inhibitory concentration (NIC) values. J Appl Microbiol. 2000;88:784–90.CAS
PubMed
Article
PubMed Central
Google Scholar
47.Sonnet P, Izard D, Mullié C. Prevalence of efflux-mediated ciprofloxacin and levofloxacin resistance in recent clinical isolates of Pseudomonas aeruginosa and its reversal by the efflux pump inhibitors 1-(1-naphthylmethyl)-piperazine and phenylalanine-arginine-β-naphthylamide. Int J Antimicrobial Agents. 2012;39:77–80.CAS
Article
Google Scholar
48.Lindgren PK, Karlsson Å, Hughes D. Mutation Rate and Evolution of Fluoroquinolone Resistance in Escherichia coli Isolates from Patients with Urinary Tract Infections. Antimicrobial Agents Chemother. 2003;47:3222–32.CAS
Article
Google Scholar
49.Klaus W, Ross A, Gsell B, Senn H. Backbone resonance assignment of the N-terminal 24 kDa fragment of the gyrase B subunit from S. aureus complexed with novobiocin. J Biomol NMR. 2000;16:357–8.CAS
PubMed
Article
PubMed Central
Google Scholar
50.Müller RT, Pos KM. The assembly and disassembly of the AcrAB-TolC three-component multidrug efflux pump. Biol Chem. 2015;396:1083–9.PubMed
Article
CAS
PubMed Central
Google Scholar
51.Oethinger M, Podglajen I, Kern WV, Levy SB. Overexpression of the marA or soxS Regulatory Gene in Clinical Topoisomerase Mutants of Escherichia coli. Antimicrob Agents Chemother. 1998;42:2089–94.CAS
PubMed
PubMed Central
Article
Google Scholar
52.Praski Alzrigat L, Huseby DL, Brandis G, Hughes D. Fitness cost constrains the spectrum of marR mutations in ciprofloxacin-resistant Escherichia coli. J Antimicrob Chemother. 2017;72:3016–24.PubMed
PubMed Central
Article
CAS
Google Scholar
53.Srikumar R, Paul CJ, Poole K. Influence of Mutations in the mexR Repressor Gene on Expression of the MexA-MexB-OprM Multidrug Efflux System of Pseudomonas aeruginosa. J Bacteriol. 2000;182:1410–4.CAS
PubMed
PubMed Central
Article
Google Scholar
54.Sánchez P, Rojo F, Martı́nez JL. Transcriptional regulation of mexR, the repressor of Pseudomonas aeruginosa mexAB-oprM multidrug efflux pump. FEMS Microbiol Lett. 2002;207:63–68.PubMed
Article
PubMed Central
Google Scholar
55.Fukuda H, Hosaka M, Hirai K, Iyobe S. New norfloxacin resistance gene in Pseudomonas aeruginosa PAO. Antimicrobial Agents Chemother. 1990;34:1757–61.CAS
Article
Google Scholar
56.Fukuda H, Hosaka M, Iyobe S, Gotoh N, Nishino T, Hirai K. nfxC-type quinolone resistance in a clinical isolate of Pseudomonas aeruginosa. Antimicrobial Agents Chemother. 1995;39:790–2.CAS
Article
Google Scholar
57.Fetar H, Gilmour C, Klinoski R, Daigle DM, Dean CR, Poole K. mexEF-oprN Multidrug Efflux Operon of Pseudomonas aeruginosa: Regulation by the MexT Activator in Response to Nitrosative Stress and Chloramphenicol. Antimicrobial Agents Chemother. 2011;55:508–14.CAS
Article
Google Scholar
58.Köhler T, Michea-Hamzehpour M, Plesiat P, Kahr AL, Pechere JC. Differential selection of multidrug efflux systems by quinolones in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1997;41:2540–3.PubMed
PubMed Central
Article
Google Scholar
59.Galajda P, Keymer J, Dalland J, Park S, Kou S, Austin R. Funnel ratchets in biology at low Reynolds number: choanotaxis. J Mod Opt. 2008;55:3413–22.CAS
Article
Google Scholar
60.Alcalde-Rico M, Hernando-Amado S, Blanco P, Martínez JL. Multidrug Efflux Pumps at the Crossroad between Antibiotic Resistance and Bacterial Virulence. Front Microbiol. 2016;7:1483.PubMed
PubMed Central
Article
Google Scholar
61.Lomovskaya O, Warren MS, Lee A, Galazzo J, Fronko R, Lee M, et al. Identification and Characterization of Inhibitors of Multidrug Resistance Efflux Pumps in Pseudomonas aeruginosa: novel Agents for Combination Therapy. Antimicrobial Agents Chemother. 2001;45:105–16.CAS
Article
Google Scholar
62.Pannek S, Higgins PG, Steinke P, Jonas D, Akova M, Bohnert JA, et al. Multidrug efflux inhibition in Acinetobacter baumannii: comparison between 1-(1-naphthylmethyl)-piperazine and phenyl-arginine-beta-naphthylamide. J Antimicrob Chemother. 2006;57:970–4.CAS
PubMed
Article
PubMed Central
Google Scholar
63.Deng J, Zhou L, Sanford RA, Shechtman LA, Dong Y, Alcalde RE, et al. Adaptive Evolution of Escherichia coli to Ciprofloxacin in Controlled Stress Environments: Contrasting Patterns of Resistance in Spatially Varying versus Uniformly Mixed Concentration Conditions. Environ Sci Technol. 2019;53:7996–8005.CAS
PubMed
Article
PubMed Central
Google Scholar
64.Olivares J, Álvarez-Ortega C, Martinez JL. Metabolic Compensation of Fitness Costs Associated with Overexpression of the Multidrug Efflux Pump MexEF-OprN in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2014;58:3904–13.PubMed
PubMed Central
Article
CAS
Google Scholar
65.Barbosa TM, Levy SB. The impact of antibiotic use on resistance development and persistence. Drug Resist Updates. 2000;3:303–11.Article
Google Scholar
66.Chia HE, Marsh ENG, Biteen JS. Extending fluorescence microscopy into anaerobic environments. Curr Opin Chem Biol. 2019;51:98–104.CAS
PubMed
Article
PubMed Central
Google Scholar
67.Laverman AM, Cazier T, Yan C, Roose-Amsaleg C, Petit F, Garnier J, et al. Exposure to vancomycin causes a shift in the microbial community structure without affecting nitrate reduction rates in river sediments. Environ Sci Pollut Res. 2015;22:13702–9.CAS
Article
Google Scholar
68.Li J, Romine MF, Ward MJ. Identification and analysis of a highly conserved chemotaxis gene cluster in Shewanella species. FEMS Microbiol Lett. 2007;273:180–6.CAS
PubMed
Article
PubMed Central
Google Scholar More