{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T11:13:38Z","timestamp":1791458018832,"version":"4.3.4"},"reference-count":79,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T00:00:00Z","timestamp":1736726400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T00:00:00Z","timestamp":1736726400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Egyptian Atomic Energy Authority"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Microbiol"],"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>One of the main issues facing public health with microbial infections is antibiotic resistance. Nanoparticles (NPs) are among the best alternatives to overcome this issue. Silver nanoparticle (AgNPs) preparations are widely applied to treat multidrug-resistant pathogens. Therefore, there is an urgent need for greater knowledge regarding the effects of improper and excessive use of these medications. The current study describes the consequences of long-term exposure to sub-lethal concentrations of AgNPs on the bacterial sensitivity to NPs and the reflection of this change on the bacterial genome.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>Chemical methods have been used to prepare AgNPs and gamma irradiation has been utilized to produce more stable AgNPs. Different techniques were used to characterize and identify the prepared AgNPs including UV-visible spectrophotometer, Fourier Transform Infrared (FT-IR), Dynamic light scattering (DLS), and zeta potential. Transmission electron microscope (TEM) and Scanning electron microscope (SEM) showed 50\u2013100\u00a0nm spherical-shaped AgNPs. Eleven gram-negative and gram-positive bacterial isolates were collected from different wound infections. The minimum inhibitory concentrations (MICs) of AgNPs against the tested isolates were evaluated using the agar dilution method. This was followed by the induction of bacterial resistance to AgNPs using increasing concentrations of AgNPs. All isolates changed their susceptibility level to become resistant to high concentrations of AgNPs upon recultivation at increasing concentrations of AgNPs. Whole genome sequencing (WGS) was performed on selected susceptible isolates of gram-positive <jats:italic>Staphylococcus lentus<\/jats:italic> (St.L.1), gram-negative <jats:italic>Klebsiella pneumonia<\/jats:italic> (KP.1), and their resistant isolates St.L_R.Ag and KP_R.Ag to detect the genomic changes and mutations.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusions<\/jats:title>\n            <jats:p>For the detection of single-nucleotide polymorphisms (SNPs) and the identification of all variants (SNPs, insertions, and deletions) in our isolates, the Variation Analysis Service tool available in the Bacterial and Viral Bioinformatics Resource Center (BV-BRC) was used. Compared to the susceptible isolates, the AgNPs-resistant isolates St.L_R.Ag and KP_R.Ag had unique mutations in specific efflux pump systems, stress response, outer membrane proteins, and permeases. These findings might help to explain how single-nucleotide variants contribute to AgNPs resistance. Consequently, strict regulations and rules regarding the use and disposal of nano waste worldwide, strict knowledge of microbe-nanoparticle interaction, and the regulated disposal of NPs are required to prevent pathogens from developing nanoparticle resistance.<\/jats:p>\n          <\/jats:sec>","DOI":"10.1186\/s12866-024-03682-x","type":"journal-article","created":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T07:29:26Z","timestamp":1736753366000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Genetic determinants of silver nanoparticle resistance and the impact of gamma irradiation on nanoparticle stability"],"prefix":"10.1186","volume":"25","author":[{"given":"Amira M.","family":"Mahfouz","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Walaa A.","family":"Eraqi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hala Nour El Din","family":"El Hifnawi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alaa El Din","family":"Shawky","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Reham","family":"Samir","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed A.","family":"Ramadan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,1,13]]},"reference":[{"issue":"10325","key":"3682_CR1","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1016\/S0140-6736(21)02724-0","volume":"399","author":"CJ Murray","year":"2022","unstructured":"Murray CJ, Ikuta KS, Sharara F, Swetschinski L, Aguilar GR, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629\u201355.","journal-title":"Lancet"},{"key":"3682_CR2","doi-asserted-by":"crossref","unstructured":"Ranjbar R, Alam M, Antimicrobial Resistance C. (2022). Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Evidence-Based Nursing. 2024;27(1):16-.","DOI":"10.1136\/ebnurs-2022-103540"},{"key":"3682_CR3","doi-asserted-by":"publisher","first-page":"1102615","DOI":"10.3389\/fmicb.2023.1102615","volume":"14","author":"S Kamat","year":"2023","unstructured":"Kamat S, Kumari M. Emergence of microbial resistance against nanoparticles: mechanisms and strategies. Front Microbiol. 2023;14:1102615.","journal-title":"Front Microbiol"},{"issue":"2","key":"3682_CR4","doi-asserted-by":"publisher","first-page":"e068122","DOI":"10.1136\/bmjopen-2022-068122","volume":"13","author":"VF Bratti","year":"2023","unstructured":"Bratti VF, Wilson BE, Fazelzad R, Pabani A, Zurn SJ, Johnson S, et al. Scoping review protocol on the impact of antimicrobial resistance on cancer management and outcomes. BMJ open. 2023;13(2):e068122.","journal-title":"BMJ open"},{"issue":"1","key":"3682_CR5","doi-asserted-by":"publisher","first-page":"104640","DOI":"10.1016\/j.idnow.2022.12.005","volume":"53","author":"A Biguenet","year":"2023","unstructured":"Biguenet A, Bouxom H, Bertrand X, Slekovec C. Antibiotic resistance in elderly patients: comparison of Enterobacterales causing urinary tract infections between community, nursing homes and hospital settings. Infect Dis Now. 2023;53(1):104640.","journal-title":"Infect Dis Now"},{"key":"3682_CR6","unstructured":"Organization WH. Global antimicrobial resistance surveillance system: manual for early implementation. World Health Organization; 2015."},{"issue":"2","key":"3682_CR7","doi-asserted-by":"publisher","first-page":"e0297921","DOI":"10.1371\/journal.pone.0297921","volume":"19","author":"S Ajulo","year":"2024","unstructured":"Ajulo S, Awosile B. Global antimicrobial resistance and use surveillance system (GLASS 2022): investigating the relationship between antimicrobial resistance and antimicrobial consumption data across the participating countries. PLoS ONE. 2024;19(2):e0297921.","journal-title":"PLoS ONE"},{"issue":"2","key":"3682_CR8","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1016\/j.jconrel.2011.07.002","volume":"156","author":"AJ Huh","year":"2011","unstructured":"Huh AJ, Kwon YJ. Nanoantibiotics: a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J Controlled Release. 2011;156(2):128\u201345.","journal-title":"J Controlled Release"},{"issue":"11","key":"3682_CR9","doi-asserted-by":"publisher","first-page":"2808","DOI":"10.3390\/ijms20112808","volume":"20","author":"N Ni\u00f1o-Mart\u00ednez","year":"2019","unstructured":"Ni\u00f1o-Mart\u00ednez N, Salas Orozco MF, Mart\u00ednez-Casta\u00f1\u00f3n G-A, Torres M\u00e9ndez F, Ruiz F. Molecular mechanisms of bacterial resistance to metal and metal oxide nanoparticles. Int J Mol Sci. 2019;20(11):2808.","journal-title":"Int J Mol Sci"},{"issue":"4","key":"3682_CR10","doi-asserted-by":"publisher","first-page":"478","DOI":"10.1016\/j.nantod.2014.06.003","volume":"9","author":"X Zhu","year":"2014","unstructured":"Zhu X, Radovic-Moreno AF, Wu J, Langer R, Shi J. Nanomedicine in the management of microbial infection\u2013overview and perspectives. Nano Today. 2014;9(4):478\u201398.","journal-title":"Nano Today"},{"key":"3682_CR11","doi-asserted-by":"publisher","first-page":"1352","DOI":"10.1007\/s13346-021-00966-x","volume":"11","author":"W Fan","year":"2021","unstructured":"Fan W, Han H, Chen Y, Zhang X, Gao Y, Li S, et al. Antimicrobial nanomedicine for ocular bacterial and fungal infection. Drug Delivery Translational Res. 2021;11:1352\u201375.","journal-title":"Drug Delivery Translational Res"},{"issue":"7","key":"3682_CR12","doi-asserted-by":"publisher","first-page":"908","DOI":"10.1016\/j.arabjc.2017.05.011","volume":"12","author":"I Khan","year":"2019","unstructured":"Khan I, Saeed K, Khan I, Nanoparticles. Properties, applications and toxicities. Arab J Chem. 2019;12(7):908\u201331.","journal-title":"Arab J Chem"},{"issue":"6","key":"3682_CR13","first-page":"385","volume":"9","author":"S Iravani","year":"2014","unstructured":"Iravani S, Korbekandi H, Mirmohammadi SV, Zolfaghari B. Synthesis of silver nanoparticles: chemical, physical and biological methods. Res Pharm Sci. 2014;9(6):385\u2013406.","journal-title":"Res Pharm Sci"},{"issue":"1","key":"3682_CR14","first-page":"70","volume":"14","author":"SMM Shanab","year":"2021","unstructured":"Shanab SMM, Partila AM, Ali HEA, Abdullah MA. Impact of gamma-irradiated silver nanoparticles biosynthesized from Pseudomonas aeruginosa on growth, lipid, and carbohydrates of Chlorella vulgaris and Dictyochloropsis Splendida. J Radiation Res Appl Sci. 2021;14(1):70\u201381.","journal-title":"J Radiation Res Appl Sci"},{"key":"3682_CR15","doi-asserted-by":"publisher","first-page":"107962","DOI":"10.1016\/j.radphyschem.2018.08.011","volume":"169","author":"G Flores-Rojas","year":"2020","unstructured":"Flores-Rojas G, L\u00f3pez-Saucedo F, Bucio E. Gamma-irradiation applied in the synthesis of metallic and organic nanoparticles: a short review. Radiat Phys Chem. 2020;169:107962.","journal-title":"Radiat Phys Chem"},{"key":"3682_CR16","doi-asserted-by":"crossref","unstructured":"Wang L, Hu C, Shao L. The antimicrobial activity of nanoparticles: present situation and prospects for the future. Int J Nanomed. 2017:1227\u201349.","DOI":"10.2147\/IJN.S121956"},{"key":"3682_CR17","doi-asserted-by":"crossref","unstructured":"Gurunathan S, Han JW, Dayem AA, Eppakayala V, Kim J-H. Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int J Nanomed. 2012:5901\u201314.","DOI":"10.2147\/IJN.S37397"},{"issue":"6","key":"3682_CR18","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1002\/smll.201302434","volume":"10","author":"YH Leung","year":"2014","unstructured":"Leung YH, Ng AM, Xu X, Shen Z, Gethings LA, Wong MT, et al. Mechanisms of antibacterial activity of MgO: non-ROS mediated toxicity of MgO nanoparticles towards Escherichia coli. Small. 2014;10(6):1171\u201383.","journal-title":"Small"},{"key":"3682_CR19","doi-asserted-by":"crossref","unstructured":"Nagy A, Harrison A, Sabbani S, Munson RS Jr, Dutta PK, Waldman WJ. Silver nanoparticles embedded in zeolite membranes: release of silver ions and mechanism of antibacterial action. Int J Nanomed. 2011:1833\u201352.","DOI":"10.2147\/IJN.S24019"},{"issue":"2","key":"3682_CR20","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1128\/CMR.16.2.189-208.2003","volume":"16","author":"P Gilbert","year":"2003","unstructured":"Gilbert P, McBain AJ. Potential impact of increased use of biocides in consumer products on prevalence of antibiotic resistance. Clin Microbiol Rev. 2003;16(2):189\u2013208.","journal-title":"Clin Microbiol Rev"},{"key":"3682_CR21","doi-asserted-by":"publisher","first-page":"652863","DOI":"10.3389\/fmicb.2021.652863","volume":"12","author":"O McNeilly","year":"2021","unstructured":"McNeilly O, Mann R, Hamidian M, Gunawan C. Emerging concern for silver nanoparticle resistance in Acinetobacter baumannii and other bacteria. Front Microbiol. 2021;12:652863.","journal-title":"Front Microbiol"},{"key":"3682_CR22","doi-asserted-by":"publisher","first-page":"118506","DOI":"10.1016\/j.envpol.2021.118506","volume":"293","author":"K Yonathan","year":"2022","unstructured":"Yonathan K, Mann R, Mahbub KR, Gunawan C. The impact of silver nanoparticles on microbial communities and antibiotic resistance determinants in the environment. Environ Pollut. 2022;293:118506.","journal-title":"Environ Pollut"},{"issue":"1","key":"3682_CR23","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1038\/nrg2626","volume":"11","author":"ML Metzker","year":"2010","unstructured":"Metzker ML. Sequencing technologies\u2014the next generation. Nat Rev Genet. 2010;11(1):31\u201346.","journal-title":"Nat Rev Genet"},{"issue":"4","key":"3682_CR24","doi-asserted-by":"publisher","first-page":"20380","DOI":"10.2807\/ese.18.04.20380-en","volume":"18","author":"A Sabat","year":"2013","unstructured":"Sabat A, Budimir A, Nashev D, S\u00e1-Le\u00e3o R, Van Dijl J, Laurent F, et al. ESCMID Study Group of Epidemiological Markers (ESGEM) overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveill. 2013;18(4):20380.","journal-title":"Euro Surveill"},{"issue":"2","key":"3682_CR25","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1164\/rccm.200812-1943OC","volume":"180","author":"A Bragonzi","year":"2009","unstructured":"Bragonzi A, Paroni M, Nonis A, Cramer N, Montanari S, Rejman J, et al. Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am J Respir Crit Care Med. 2009;180(2):138\u201345.","journal-title":"Am J Respir Crit Care Med"},{"issue":"5","key":"3682_CR26","doi-asserted-by":"publisher","first-page":"2214","DOI":"10.1128\/IAI.01282-06","volume":"75","author":"L Jelsbak","year":"2007","unstructured":"Jelsbak L, Johansen HK, Frost A-L, Th\u00f8gersen R, Thomsen LE, Ciofu O, et al. Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect Immun. 2007;75(5):2214\u201324.","journal-title":"Infect Immun"},{"key":"3682_CR27","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1039\/df9511100055","volume":"11","author":"J Turkevich","year":"1951","unstructured":"Turkevich J, Stevenson PC, Hillier J. A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss Faraday Soc. 1951;11:55\u201375.","journal-title":"Discuss Faraday Soc"},{"issue":"17","key":"3682_CR28","doi-asserted-by":"publisher","first-page":"3391","DOI":"10.1021\/j100214a025","volume":"86","author":"P Lee","year":"1982","unstructured":"Lee P, Meisel D. Adsorption and surface-enhanced Raman of dyes on silver and gold sols. J Phys Chem. 1982;86(17):3391\u20135.","journal-title":"J Phys Chem"},{"issue":"1","key":"3682_CR29","first-page":"4","volume":"45","author":"J Kok","year":"2013","unstructured":"Kok J, Chen SC, Dwyer DE, Iredell JR. Current status of matrix-assisted laser desorption ionisation-time of flight mass spectrometry in the clinical microbiology laboratory. Pathology-Journal RCPA. 2013;45(1):4\u201317.","journal-title":"Pathology-Journal RCPA"},{"issue":"20","key":"3682_CR30","doi-asserted-by":"publisher","first-page":"4775","DOI":"10.3390\/molecules25204775","volume":"25","author":"S Tsuchida","year":"2020","unstructured":"Tsuchida S, Umemura H, Nakayama T. Current status of matrix-assisted laser desorption\/ionization\u2013time-of-flight mass spectrometry (MALDI-TOF MS) in clinical diagnostic microbiology. Molecules. 2020;25(20):4775.","journal-title":"Molecules"},{"key":"3682_CR31","doi-asserted-by":"crossref","unstructured":"Humphries R, Ambler J, Mitchell S, Castanheira M, Dingle T, Hindler J, on behalf of the CLSI Methods Development and Standardization Working Group of the Subcommittee on Antimicrobial Susceptibility Testing. 2018. CLSI Methods Development and Standardization Working Group best practices for evaluation of antimicrobial susceptibility tests. J Clin Microbiol. 2018;56:01934.","DOI":"10.1128\/JCM.01934-17"},{"key":"3682_CR32","unstructured":"Wayne P. Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing. 2011."},{"issue":"1","key":"3682_CR33","doi-asserted-by":"publisher","first-page":"2561","DOI":"10.1038\/s41467-022-30269-9","volume":"13","author":"F Tesson","year":"2022","unstructured":"Tesson F, Herv\u00e9 A, Mordret E, Touchon M, D\u2019humi\u00e8res C, Cury J, et al. Systematic and quantitative view of the antiviral arsenal of prokaryotes. Nat Commun. 2022;13(1):2561.","journal-title":"Nat Commun"},{"key":"3682_CR34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2164-9-75","volume":"9","author":"RK Aziz","year":"2008","unstructured":"Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:1\u201315.","journal-title":"BMC Genomics"},{"issue":"1","key":"3682_CR35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep08365","volume":"5","author":"T Brettin","year":"2015","unstructured":"Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep. 2015;5(1):1\u20136.","journal-title":"Sci Rep"},{"issue":"4","key":"3682_CR36","doi-asserted-by":"publisher","first-page":"582","DOI":"10.1128\/CMR.00040-09","volume":"22","author":"PD Lister","year":"2009","unstructured":"Lister PD, Wolter DJ, Hanson ND. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin Microbiol Rev. 2009;22(4):582\u2013610.","journal-title":"Clin Microbiol Rev"},{"issue":"D1","key":"3682_CR37","doi-asserted-by":"publisher","first-page":"D641","DOI":"10.1093\/nar\/gkr989","volume":"40","author":"L Chen","year":"2012","unstructured":"Chen L, Xiong Z, Sun L, Yang J, Jin Q. VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res. 2012;40(D1):D641\u20135.","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"3682_CR38","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1093\/emph\/eow016","volume":"2016","author":"G Jansen","year":"2016","unstructured":"Jansen G, Mahrt N, Tueffers L, Barbosa C, Harjes M, Adolph G, et al. Association between clinical antibiotic resistance and susceptibility of Pseudomonas in the cystic fibrosis lung. Evol Med Public Health. 2016;2016(1):182\u201394.","journal-title":"Evol Med Public Health"},{"key":"3682_CR39","doi-asserted-by":"publisher","first-page":"42","DOI":"10.3389\/fgene.2015.00042","volume":"6","author":"JL Graves Jr","year":"2015","unstructured":"Graves JL Jr, Tajkarimi M, Cunningham Q, Campbell A, Nonga H, Harrison SH, et al. Rapid evolution of silver nanoparticle resistance in Escherichia coli. Front Genet. 2015;6:42.","journal-title":"Front Genet"},{"issue":"12","key":"3682_CR40","doi-asserted-by":"publisher","first-page":"2003090","DOI":"10.1002\/advs.202003090","volume":"8","author":"D Pan\u00e1\u010dek","year":"2021","unstructured":"Pan\u00e1\u010dek D, Hochvaldov\u00e1 L, Bakandritsos A, Malina T, Langer M, Belza J, et al. Silver covalently bound to cyanographene overcomes bacterial resistance to silver nanoparticles and antibiotics. Adv Sci. 2021;8(12):2003090.","journal-title":"Adv Sci"},{"issue":"5","key":"3682_CR41","first-page":"166","volume":"5","author":"SM Gamboa","year":"2019","unstructured":"Gamboa SM, Rojas E, Mart\u00ednez V, Vega-Baudrit J. Synthesis and characterization of silver nanoparticles and their application as an antibacterial agent. Int J Biosen Bioelectron. 2019;5(5):166\u201373.","journal-title":"Int J Biosen Bioelectron"},{"issue":"1","key":"3682_CR42","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/j.kijoms.2017.10.007","volume":"4","author":"G Lakshmanan","year":"2018","unstructured":"Lakshmanan G, Sathiyaseelan A, Kalaichelvan P, Murugesan K. Plant-mediated synthesis of silver nanoparticles using fruit extract of Cleome viscosa L.: assessment of their antibacterial and anticancer activity. Karbala Int J Mod Sci. 2018;4(1):61\u20138.","journal-title":"Karbala Int J Mod Sci"},{"issue":"1","key":"3682_CR43","first-page":"4213275","volume":"2017","author":"K Jemal","year":"2017","unstructured":"Jemal K, Sandeep B, Pola S. Synthesis, characterization, and evaluation of the antibacterial activity of Allophylus Serratus leaf and leaf derived callus extracts mediated silver nanoparticles. J Nanomaterials. 2017;2017(1):4213275.","journal-title":"J Nanomaterials"},{"issue":"10","key":"3682_CR44","doi-asserted-by":"publisher","first-page":"2346","DOI":"10.1088\/0957-4484\/16\/10\/059","volume":"16","author":"JR Morones","year":"2005","unstructured":"Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ram\u00edrez JT, et al. The bactericidal effect of silver nanoparticles. Nanotechnology. 2005;16(10):2346.","journal-title":"Nanotechnology"},{"key":"3682_CR45","doi-asserted-by":"publisher","first-page":"379304","DOI":"10.3389\/fmicb.2018.01555","volume":"9","author":"YY Loo","year":"2018","unstructured":"Loo YY, Rukayadi Y, Nor-Khaizura M-A-R, Kuan CH, Chieng BW, Nishibuchi M, et al. In vitro antimicrobial activity of green synthesized silver nanoparticles against selected gram-negative foodborne pathogens. Front Microbiol. 2018;9:379304.","journal-title":"Front Microbiol"},{"issue":"12","key":"3682_CR46","doi-asserted-by":"publisher","first-page":"1775","DOI":"10.3390\/nano9121775","volume":"9","author":"RE Duval","year":"2019","unstructured":"Duval RE, Gouyau J, Lamouroux E. Limitations of recent studies dealing with the antibacterial properties of silver nanoparticles: Fact and opinion. Nanomaterials. 2019;9(12):1775.","journal-title":"Nanomaterials"},{"issue":"1","key":"3682_CR47","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1038\/s41565-017-0013-y","volume":"13","author":"A Pan\u00e1\u010dek","year":"2018","unstructured":"Pan\u00e1\u010dek A, Kv\u00edtek L, Sm\u00e9kalov\u00e1 M, Ve\u010de\u0159ov\u00e1 R, Kol\u00e1\u0159 M, R\u00f6derov\u00e1 M, et al. Bacterial resistance to silver nanoparticles and how to overcome it. Nat Nanotechnol. 2018;13(1):65\u201371.","journal-title":"Nat Nanotechnol"},{"issue":"6","key":"3682_CR48","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1016\/j.cell.2007.03.004","volume":"128","author":"MN Alekshun","year":"2007","unstructured":"Alekshun MN, Levy SB. Molecular mechanisms of antibacterial multidrug resistance. Cell. 2007;128(6):1037\u201350.","journal-title":"Cell"},{"issue":"2","key":"3682_CR49","doi-asserted-by":"publisher","first-page":"77","DOI":"10.2174\/1389201023378454","volume":"3","author":"K Poole","year":"2002","unstructured":"Poole K. Outer membranes and efflux: the path to multidrug resistance in Gram-negative bacteria. Curr Pharm Biotechnol. 2002;3(2):77\u201398.","journal-title":"Curr Pharm Biotechnol"},{"issue":"1","key":"3682_CR50","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1093\/jac\/dki171","volume":"56","author":"K Poole","year":"2005","unstructured":"Poole K. Efflux-mediated antimicrobial resistance. J Antimicrob Chemother. 2005;56(1):20\u201351.","journal-title":"J Antimicrob Chemother"},{"issue":"4","key":"3682_CR51","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1128\/MMBR.64.4.672-693.2000","volume":"64","author":"M Putman","year":"2000","unstructured":"Putman M, van Veen HW, Konings WN. Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Rev. 2000;64(4):672\u201393.","journal-title":"Microbiol Mol Biol Rev"},{"issue":"5","key":"3682_CR52","doi-asserted-by":"publisher","first-page":"834","DOI":"10.1016\/j.bbapap.2009.02.002","volume":"1794","author":"K Nishino","year":"2009","unstructured":"Nishino K, Nikaido E, Yamaguchi A. Regulation and physiological function of multidrug efflux pumps in Escherichia coli and Salmonella. Biochim et Biophys Acta (BBA)-Proteins Proteom. 2009;1794(5):834\u201343.","journal-title":"Biochim et Biophys Acta (BBA)-Proteins Proteom"},{"issue":"1","key":"3682_CR53","doi-asserted-by":"publisher","first-page":"01982","DOI":"10.1128\/mbio","volume":"6","author":"KA Hassan","year":"2015","unstructured":"Hassan KA, Liu Q, Henderson PJ, Paulsen IT. Homologs of the Acinetobacter baumannii AceI transporter represent a new family of bacterial multidrug efflux systems. MBio. 2015;6(1):01982\u201314. https:\/\/doi.org\/10.1128\/mbio.","journal-title":"MBio"},{"key":"3682_CR54","doi-asserted-by":"publisher","unstructured":"Kornelsen V, Kumar A. Update on multidrug resistance efflux pumps in Acinetobacter Spp. Antimicrob Agents Chemother. 2021;65(7). https:\/\/doi.org\/10.1128\/aac. 00514\u2009\u2013\u200921.","DOI":"10.1128\/aac"},{"key":"3682_CR55","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1146\/annurev.micro.61.080706.093329","volume":"62","author":"CJ Law","year":"2008","unstructured":"Law CJ, Maloney PC, Wang D-N. Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol. 2008;62:289\u2013305.","journal-title":"Annu Rev Microbiol"},{"issue":"2","key":"3682_CR56","first-page":"145","volume":"3","author":"IT Paulsen","year":"2001","unstructured":"Paulsen IT, Chen J, Nelson KE, Saier MH Jr. Comparative genomics of microbial drug efflux systems. J Mol Microbiol Biotechnol. 2001;3(2):145\u201350.","journal-title":"J Mol Microbiol Biotechnol"},{"issue":"1","key":"3682_CR57","first-page":"7630316","volume":"2019","author":"M Salas-Orozco","year":"2019","unstructured":"Salas-Orozco M, Ni\u00f1o-Mart\u00ednez N, Mart\u00ednez-Casta\u00f1\u00f3n G-A, M\u00e9ndez FT, Jasso MEC, Ruiz F. Mechanisms of resistance to silver nanoparticles in endodontic bacteria: a literature review. J Nanomaterials. 2019;2019(1):7630316.","journal-title":"J Nanomaterials"},{"issue":"19","key":"3682_CR58","doi-asserted-by":"publisher","first-page":"5891","DOI":"10.1128\/JB.181.19.5891-5897.1999","volume":"181","author":"C Rensing","year":"1999","unstructured":"Rensing C, Ghosh M, Rosen BP. Families of soft-metal-ion-transporting ATPases. J Bacteriol. 1999;181(19):5891\u20137.","journal-title":"J Bacteriol"},{"issue":"5","key":"3682_CR59","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1111\/j.1365-2958.1994.tb00362.x","volume":"11","author":"M Saier Jr","year":"1994","unstructured":"Saier M Jr, Tam R, Reizer A, Reizer J. Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol. 1994;11(5):841\u20137.","journal-title":"Mol Microbiol"},{"issue":"27","key":"3682_CR60","doi-asserted-by":"publisher","first-page":"22298","DOI":"10.1021\/acsami.7b06433","volume":"9","author":"J Guo","year":"2017","unstructured":"Guo J, Gao S-H, Lu J, Bond PL, Verstraete W, Yuan Z. Copper oxide nanoparticles induce lysogenic bacteriophage and metal-resistance genes in Pseudomonas aeruginosa PAO1. ACS Appl Mater Interfaces. 2017;9(27):22298\u2013307.","journal-title":"ACS Appl Mater Interfaces"},{"issue":"7","key":"3682_CR61","doi-asserted-by":"publisher","first-page":"6091","DOI":"10.1021\/nn3011619","volume":"6","author":"Y Yang","year":"2012","unstructured":"Yang Y, Mathieu JM, Chattopadhyay S, Miller JT, Wu T, Shibata T, et al. Defense mechanisms of Pseudomonas aeruginosa PAO1 against quantum dots and their released heavy metals. ACS Nano. 2012;6(7):6091\u20138.","journal-title":"ACS Nano"},{"issue":"13","key":"3682_CR62","doi-asserted-by":"publisher","first-page":"3804","DOI":"10.1128\/JB.185.13.3804-3812.2003","volume":"185","author":"S Franke","year":"2003","unstructured":"Franke S, Grass G, Rensing C, Nies DH. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol. 2003;185(13):3804\u201312.","journal-title":"J Bacteriol"},{"issue":"6","key":"3682_CR63","doi-asserted-by":"publisher","first-page":"2351","DOI":"10.1021\/pr700646b","volume":"7","author":"C-N Lok","year":"2008","unstructured":"Lok C-N, Ho C-M, Chen R, Tam PK-H, Chiu J-F, Che C-M. Proteomic identification of the Cus system as a major determinant of constitutive Escherichia coli silver resistance of chromosomal origin. J Proteome Res. 2008;7(6):2351\u20136.","journal-title":"J Proteome Res"},{"issue":"4","key":"3682_CR64","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1093\/jac\/dku523","volume":"70","author":"CP Randall","year":"2015","unstructured":"Randall CP, Gupta A, Jackson N, Busse D, O\u2019Neill AJ. Silver resistance in Gram-negative bacteria: a dissection of endogenous and exogenous mechanisms. J Antimicrob Chemother. 2015;70(4):1037\u201346.","journal-title":"J Antimicrob Chemother"},{"issue":"2","key":"3682_CR65","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1016\/S0005-2736(99)00158-3","volume":"1461","author":"J Young","year":"1999","unstructured":"Young J, Holland IB. ABC transporters: bacterial exporters-revisited five years on. Biochim et Biophys Acta (BBA)-Biomembranes. 1999;1461(2):177\u2013200.","journal-title":"Biochim et Biophys Acta (BBA)-Biomembranes"},{"issue":"8","key":"3682_CR66","doi-asserted-by":"publisher","first-page":"3412","DOI":"10.1128\/IAI.01543-08","volume":"77","author":"S Basavanna","year":"2009","unstructured":"Basavanna S, Khandavilli S, Yuste J, Cohen JM, Hosie AH, Webb AJ, et al. Screening of Streptococcus pneumoniae ABC transporter mutants demonstrates that LivJHMGF, a branched-chain amino acid ABC transporter, is necessary for disease pathogenesis. Infect Immun. 2009;77(8):3412\u201323.","journal-title":"Infect Immun"},{"key":"3682_CR67","doi-asserted-by":"publisher","first-page":"105734","DOI":"10.1016\/j.micpath.2022.105734","volume":"171","author":"AA Akhtar","year":"2022","unstructured":"Akhtar AA, Turner DP. The role of bacterial ATP-binding cassette (ABC) transporters in pathogenesis and virulence: therapeutic and vaccine potential. Microb Pathog. 2022;171:105734.","journal-title":"Microb Pathog"},{"issue":"11","key":"3682_CR68","doi-asserted-by":"publisher","first-page":"4681","DOI":"10.1021\/acsabm.9b00614","volume":"2","author":"J Jose","year":"2019","unstructured":"Jose J, Anas A, Jose B, Puthirath AB, Athiyanathil S, Jasmin C, et al. Extinction of antimicrobial resistant pathogens using silver embedded silica nanoparticles and an efflux pump blocker. ACS Appl Bio Mater. 2019;2(11):4681\u20136.","journal-title":"ACS Appl Bio Mater"},{"issue":"1","key":"3682_CR69","first-page":"204141","volume":"2013","author":"S Kumar","year":"2013","unstructured":"Kumar S, Mukherjee MM, Varela MF. Modulation of bacterial multidrug resistance efflux pumps of the major facilitator superfamily. Int J Bacteriol. 2013;2013(1):204141.","journal-title":"Int J Bacteriol"},{"issue":"1","key":"3682_CR70","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1186\/s12866-022-02514-0","volume":"22","author":"X Wang","year":"2022","unstructured":"Wang X, Zhang Y, Li C, Li G, Wu D, Li T, et al. Antimicrobial resistance of Escherichia coli, Enterobacter spp., Klebsiella pneumoniae and Enterococcus spp. isolated from the feces of giant panda. BMC Microbiol. 2022;22(1):102.","journal-title":"BMC Microbiol"},{"issue":"1","key":"3682_CR71","doi-asserted-by":"publisher","first-page":"678","DOI":"10.1038\/s42003-021-02213-y","volume":"4","author":"C Pagnout","year":"2021","unstructured":"Pagnout C, Razafitianamaharavo A, Sohm B, Caillet C, Beaussart A, Delatour E, et al. Osmotic stress and vesiculation as key mechanisms controlling bacterial sensitivity and resistance to TiO2 nanoparticles. Commun Biology. 2021;4(1):678.","journal-title":"Commun Biology"},{"issue":"12","key":"3682_CR72","doi-asserted-by":"publisher","first-page":"183154","DOI":"10.1016\/j.bbamem.2019.183154","volume":"1862","author":"T Kusakizako","year":"2020","unstructured":"Kusakizako T, Miyauchi H, Ishitani R, Nureki O. Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochim et Biophys Acta (BBA)-biomembranes. 2020;1862(12):183154.","journal-title":"Biochim et Biophys Acta (BBA)-biomembranes"},{"key":"3682_CR73","doi-asserted-by":"publisher","unstructured":"Rouquette-Loughlin CE, Dhulipala V, Reimche JL, Raterman E, Begum AA, Jerse AE, et al. cis-and trans-acting factors influence expression of the norm-encoded efflux pump of Neisseria gonorrhoeae and levels of Gonococcal susceptibility to substrate antimicrobials. Antimicrob Agents Chemother. 2018;62(8). https:\/\/doi.org\/10.1128\/aac. 00821\u2009\u2013\u200918.","DOI":"10.1128\/aac"},{"issue":"4","key":"3682_CR74","doi-asserted-by":"publisher","first-page":"520","DOI":"10.3390\/antibiotics11040520","volume":"11","author":"L Huang","year":"2022","unstructured":"Huang L, Wu C, Gao H, Xu C, Dai M, Huang L, et al. Bacterial multidrug efflux pumps at the frontline of antimicrobial resistance: an overview. Antibiotics. 2022;11(4):520.","journal-title":"Antibiotics"},{"issue":"4","key":"3682_CR75","doi-asserted-by":"publisher","first-page":"e1003421","DOI":"10.1371\/journal.pgen.1003421","volume":"9","author":"Z Baharoglu","year":"2013","unstructured":"Baharoglu Z, Krin E, Mazel D. RpoS plays a central role in the SOS induction by sub-lethal aminoglycoside concentrations in Vibrio cholerae. PLoS Genet. 2013;9(4):e1003421.","journal-title":"PLoS Genet"},{"key":"3682_CR76","doi-asserted-by":"crossref","unstructured":"Long H, Miller SF, Strauss C, Zhao C, Cheng L, Ye Z et al. Antibiotic treatment enhances the genome-wide mutation rate of target cells. Proceedings of the National Academy of Sciences. 2016;113(18):E2498-E505.","DOI":"10.1073\/pnas.1601208113"},{"issue":"9","key":"3682_CR77","doi-asserted-by":"publisher","first-page":"2961","DOI":"10.1128\/JB.185.9.2961-2966.2003","volume":"185","author":"GT Robertson","year":"2003","unstructured":"Robertson GT, Ng W-L, Gilmour R, Winkler ME. Essentiality of clpX, but not clpP, clpL, clpC, or clpE, in Streptococcus pneumoniae R6. J Bacteriol. 2003;185(9):2961\u20136.","journal-title":"J Bacteriol"},{"issue":"15","key":"3682_CR78","doi-asserted-by":"publisher","first-page":"5964","DOI":"10.1021\/es100679f","volume":"44","author":"N Gou","year":"2010","unstructured":"Gou N, Onnis-Hayden A, Gu AZ. Mechanistic toxicity assessment of nanomaterials by whole-cell-array stress genes expression analysis. Environ Sci Technol. 2010;44(15):5964\u201370.","journal-title":"Environ Sci Technol"},{"issue":"6","key":"3682_CR79","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1038\/nrmicro3028","volume":"11","author":"JA Lemire","year":"2013","unstructured":"Lemire JA, Harrison JJ, Turner RJ. Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol. 2013;11(6):371\u201384.","journal-title":"Nat Rev Microbiol"}],"container-title":["BMC Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12866-024-03682-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12866-024-03682-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12866-024-03682-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T07:29:37Z","timestamp":1736753377000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcmicrobiol.biomedcentral.com\/articles\/10.1186\/s12866-024-03682-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,13]]},"references-count":79,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["3682"],"URL":"https:\/\/doi.org\/10.1186\/s12866-024-03682-x","relation":{},"ISSN":["1471-2180"],"issn-type":[{"value":"1471-2180","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,13]]},"assertion":[{"value":"15 July 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 November 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 January 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"18"}}