دورية أكاديمية

The role of chemotaxis and efflux pumps on nitrate reduction in the toxic regions of a ciprofloxacin concentration gradient.

التفاصيل البيبلوغرافية
العنوان: The role of chemotaxis and efflux pumps on nitrate reduction in the toxic regions of a ciprofloxacin concentration gradient.
المؤلفون: Alcalde RE; Department of Civil, Architectural, and Environmental Engineering, University of Texas at Austin, Austin, TX, USA., Dundas CM; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Dong Y; School of Environmental Studies, China University of Geosciences (Wuhan), Wuhan, Hubei, China.; Department of Geology, University of Illinois at Urbana-Champaign, Urbana, IL, USA., Sanford RA; Department of Geology, University of Illinois at Urbana-Champaign, Urbana, IL, USA., Keitz BK; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Fouke BW; Department of Geology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.; Department of Microbiology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.; Carl R. Woese Institute of Genomic Biology, University of Illinois Urbana-Champaign, Urbana, IL, USA., Werth CJ; Department of Civil, Architectural, and Environmental Engineering, University of Texas at Austin, Austin, TX, USA. werth@utexas.edu.
المصدر: The ISME journal [ISME J] 2021 Oct; Vol. 15 (10), pp. 2920-2932. Date of Electronic Publication: 2021 Apr 29.
نوع المنشور: Journal Article; Research Support, U.S. Gov't, Non-P.H.S.
اللغة: English
بيانات الدورية: Publisher: Oxford University Press Country of Publication: England NLM ID: 101301086 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1751-7370 (Electronic) Linking ISSN: 17517362 NLM ISO Abbreviation: ISME J Subsets: MEDLINE
أسماء مطبوعة: Publication: 2024- : Oxford : Oxford University Press
Original Publication: London : Nature Pub. Group
مواضيع طبية MeSH: Ciprofloxacin*/pharmacology , Nitrates*, Anti-Bacterial Agents/pharmacology ; Bacterial Proteins ; Chemotaxis ; Drug Resistance, Multiple, Bacterial ; Ecosystem ; Membrane Transport Proteins ; Microbial Sensitivity Tests ; Shewanella
مستخلص: Spatial concentration gradients of antibiotics are prevalent in the natural environment. Yet, the microbial response in these heterogeneous systems remains poorly understood. We used a microfluidic reactor to create an artificial microscopic ecosystem that generates diffusive gradients of solutes across interconnected microenvironments. With this reactor, we showed that chemotaxis toward a soluble electron acceptor (nitrate) allowed Shewanella oneidensis MR-1 to inhabit and sustain metabolic activity in highly toxic regions of the antibiotic ciprofloxacin (>80× minimum inhibitory concentration, MIC). Acquired antibiotic resistance was not observed for cells extracted from the reactor, so we explored the role of transient adaptive resistance by probing multidrug resistance (MDR) efflux pumps, ancient elements that are important for bacterial physiology and virulence. Accordingly, we constructed an efflux pump deficient mutant (∆mexF) and used resistance-nodulation-division (RND) efflux pump inhibitors (EPIs). While batch results showed the importance of RND efflux pumps for microbial survival, microfluidic studies indicated that these pumps were not necessary for survival in antibiotic gradients. Our work contributes to an emerging body of knowledge deciphering the effects of antibiotic spatial heterogeneity on microorganisms and highlights differences of microbial response in these systems versus well-mixed batch conditions.
(© 2021. The Author(s), under exclusive licence to International Society for Microbial Ecology.)
References: DeVries SL, Zhang P. Antibiotics and the Terrestrial Nitrogen Cycle: a review. Curr Pollut Rep. 2016;2:51–67. (PMID: 10.1007/s40726-016-0027-3)
Kümmerer K. Antibiotics in the aquatic environment – A review – Part I. Chemosphere. 2009;75:417–34. (PMID: 1918590010.1016/j.chemosphere.2008.11.086)
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. (PMID: 2706538510.2134/jeq2016.01.0023)
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. (PMID: 10.1007/s11356-015-4943-3)
Grenni P, Ancona V, Barra, Caracciolo A. Ecological effects of antibiotics on natural ecosystems: a review. Microchemical J. 2018;136:25–39. (PMID: 10.1016/j.microc.2017.02.006)
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. (PMID: 1939850710.2134/jeq2008.0128)
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. (PMID: 3254478910.1016/j.envpol.2020.114930)
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. (PMID: 3002933310.1016/j.envpol.2018.05.085)
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. (PMID: 3084140610.1016/j.scitotenv.2018.11.061)
Baquero F, Negri M-C. Challenges: selective compartments for resistant microorganisms in antibiotic gradients. BioEssays. 1997;19:731–6. (PMID: 926425610.1002/bies.950190814)
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. (PMID: 22711808339082910.1073/pnas.1117716109)
Andersson DI, Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol. 2014;12:465–78. (PMID: 2486103610.1038/nrmicro3270)
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. (PMID: 2818399610.1126/science.aaj2191)
Cohen NR, Lobritz MA, Collins JJ. Microbial Persistence and the Road to Drug Resistance. Cell Host Microbe. 2013;13:632–42. (PMID: 23768488369539710.1016/j.chom.2013.05.009)
Hughes D, Andersson DI. Environmental and genetic modulation of the phenotypic expression of antibiotic resistance. FEMS Microbiol Rev. 2017;41:374–91. (PMID: 28333270543576510.1093/femsre/fux004)
Venter H, Arzanlou M, Chai WC, Venter H. Intrinsic, adaptive and acquired antimicrobial resistance in Gram-negative bacteria. Essays Biochem. 2017;61:49–59. (PMID: 2825822910.1042/EBC20160063)
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. (PMID: 3067328610.1021/acs.est.8b04838)
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. (PMID: 2614053110.1038/ismej.2015.107)
Butler MT, Wang Q, Harshey RM. Cell density and mobility protect swarming bacteria against antibiotics. Proc Natl Acad Sci. 2010;107:3776–81. (PMID: 20133590284048310.1073/pnas.0910934107)
Steel H, Papachristodoulou A. The effect of spatiotemporal antibiotic inhomogeneities on the evolution of resistance. J Theor Biol. 2020;486:110077. (PMID: 3171518110.1016/j.jtbi.2019.110077)
Lai S, Tremblay J, Déziel E. Swarming motility: a multicellular behaviour conferring antimicrobial resistance. Environ Microbiol. 2009;11:126–36. (PMID: 1879331710.1111/j.1462-2920.2008.01747.x)
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. (PMID: 2194089910.1126/science.1208747)
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. (PMID: 24046372379173510.1073/pnas.1314385110)
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. (PMID: 27609891553443410.1126/science.aag0822)
Alexandre G, Greer-Phillips S, Zhulin IB. Ecological role of energy taxis in microorganisms. FEMS Microbiol Rev. 2004;28:113–26. (PMID: 1497553310.1016/j.femsre.2003.10.003)
Fenchel T. Microbial Behavior in a Heterogeneous World. Science. 2002;296:1068–71. (PMID: 1200411810.1126/science.1070118)
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. (PMID: 1711432010.1128/AEM.01086-06)
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. (PMID: 1966495310.1016/j.mib.2009.07.003)
Fernández L, Hancock REW. Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance. Clin Microbiol Rev. 2012;25:661–81. (PMID: 23034325348574910.1128/CMR.00043-12)
Alvarez-Ortega C, Olivares J, Martinez JL. RND multidrug efflux pumps: what are they good for? Front Microbiol. 2013;4:7. (PMID: 23386844356404310.3389/fmicb.2013.00007)
Anes J, McCusker MP, Fanning S, Martins M. The ins and outs of RND efflux pumps in Escherichia coli. Front Microbiol. 2015;6:587. (PMID: 26113845446210110.3389/fmicb.2015.00587)
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. (PMID: 882194010.1046/j.1365-2958.1996.357881.x)
Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev. 2003;27:313–39. (PMID: 1282927310.1016/S0168-6445(03)00048-2)
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. (PMID: 10.1128/AAC.01495-10)
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. (PMID: 2070973510.1093/jac/dkq287)
Zhang L, Mah T-F. Involvement of a Novel Efflux System in Biofilm-Specific Resistance to Antibiotics. J Bacteriol. 2008;190:4447–52. (PMID: 1846910810.1128/JB.01655-072446775)
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.
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. (PMID: 10.1590/S1984-82502011000100004)
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. (PMID: 3090896510.1016/j.chemosphere.2019.03.081)
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. (PMID: 10.1128/AAC.00101-11)
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. (PMID: 24695404410359010.1093/bioinformatics/btu170)
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. (PMID: 24838886423970110.1007/978-1-4939-0554-6_12)
Saltikov CW, Newman DK. Genetic identification of a respiratory arsenate reductase. PNAS. 2003;100:10983–8. (PMID: 1293940819691310.1073/pnas.1834303100)
Engler C, Kandzia R, Marillonnet S. A One Pot, One Step, Precision Cloning Method with High Throughput Capability. PLOS ONE. 2008;3:e3647. (PMID: 18985154257441510.1371/journal.pone.0003647)
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. (PMID: 10.1046/j.1469-0691.2003.00790.x)
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. (PMID: 1079253810.1046/j.1365-2672.2000.01017.x)
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. (PMID: 10.1016/j.ijantimicag.2011.08.005)
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. (PMID: 10.1128/AAC.47.10.3222-3232.2003)
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. (PMID: 1082689210.1023/A:1008383508219)
Müller RT, Pos KM. The assembly and disassembly of the AcrAB-TolC three-component multidrug efflux pump. Biol Chem. 2015;396:1083–9. (PMID: 2606162110.1515/hsz-2015-0150)
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. (PMID: 968741210586810.1128/AAC.42.8.2089)
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. (PMID: 28962020589070810.1093/jac/dkx270)
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. (PMID: 106714659443010.1128/JB.182.5.1410-1414.2000)
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. (PMID: 1188675210.1111/j.1574-6968.2002.tb11029.x)
Fukuda H, Hosaka M, Hirai K, Iyobe S. New norfloxacin resistance gene in Pseudomonas aeruginosa PAO. Antimicrobial Agents Chemother. 1990;34:1757–61. (PMID: 10.1128/AAC.34.9.1757)
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. (PMID: 10.1128/AAC.39.3.790)
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. (PMID: 10.1128/AAC.00830-10)
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. (PMID: 937136316415810.1128/AAC.41.11.2540)
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. (PMID: 10.1080/09500340802495826)
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. (PMID: 27708632503025210.3389/fmicb.2016.01483)
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. (PMID: 10.1128/AAC.45.1.105-116.2001)
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. (PMID: 1653142910.1093/jac/dkl081)
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. (PMID: 3126940010.1021/acs.est.9b00881)
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. (PMID: 24777101406859810.1128/AAC.00121-14)
Barbosa TM, Levy SB. The impact of antibiotic use on resistance development and persistence. Drug Resist Updates. 2000;3:303–11. (PMID: 10.1054/drup.2000.0167)
Chia HE, Marsh ENG, Biteen JS. Extending fluorescence microscopy into anaerobic environments. Curr Opin Chem Biol. 2019;51:98–104. (PMID: 3125237210.1016/j.cbpa.2019.05.008)
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. (PMID: 10.1007/s11356-015-4159-6)
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. (PMID: 1759022710.1111/j.1574-6968.2007.00810.x)
المشرفين على المادة: 0 (Anti-Bacterial Agents)
0 (Bacterial Proteins)
0 (Membrane Transport Proteins)
0 (Nitrates)
5E8K9I0O4U (Ciprofloxacin)
SCR Organism: Shewanella oneidensis
تواريخ الأحداث: Date Created: 20210430 Date Completed: 20210922 Latest Revision: 20230201
رمز التحديث: 20231215
مُعرف محوري في PubMed: PMC8443623
DOI: 10.1038/s41396-021-00975-1
PMID: 33927341
قاعدة البيانات: MEDLINE
الوصف
تدمد:1751-7370
DOI:10.1038/s41396-021-00975-1