Abstract
In this mini-review, after a brief introduction into the widespread antimicrobial use of silver ions and nanoparticles against bacteria, fungi and viruses, the toxicity of silver compounds and the molecular mechanisms of microbial silver resistance are discussed, including recent studies on bacteria and fungi. The similarities and differences between silver ions and silver nanoparticles as antimicrobial agents are also mentioned. Regarding bacterial ionic silver resistance, the roles of the sil operon, silver cation efflux proteins, and copper-silver efflux systems are explained. The importance of bacterially produced exopolysaccharides as a physiological (biofilm) defense mechanism against silver nanoparticles is also emphasized. Regarding fungal silver resistance, the roles of metallothioneins, copper-transporting P-type ATPases and cell wall are discussed. Recent evolutionary engineering (adaptive laboratory evolution) studies are also discussed which revealed that silver resistance can evolve rapidly in bacteria and fungi. The cross-resistance observed between silver resistance and resistance to other heavy metals and antibiotics in bacteria and fungi is also explained as a clinically and environmentally important issue. The use of silver against bacterial and fungal biofilm formation is also discussed. Finally, the antiviral effects of silver and the use of silver nanoparticles against SARS-CoV-2 and other viruses are mentioned. To conclude, silver compounds are becoming increasingly important as antimicrobial agents, and their widespread use necessitates detailed understanding of microbial silver response and resistance mechanisms, as well as the ecological effects of silver compounds.
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Abriat C, Gazil O, Heuzey MC et al (2021) The polymeric matrix composition of Vibrio cholerae biofilms modulate resistance to silver nanoparticles prepared by hydrothermal synthesis. ACS Appl Mater Interfaces 13:35356–35364
Abul Qais F, Samreen, Ahmad I (2018) Broad-spectrum inhibitory effect of green synthesised silver nanoparticles from Withania somnifera (L.) on microbial growth, biofilm and respiration: a putative mechanistic approach. IET Nanobiotechnol 12:325–335
Adle DJ, Sinani D, Kim H et al (2007) A cadmium-transporting P1B-type ATPase in yeast Saccharomyces cerevisiae. J Biol Chem 282::947–955
Al-Ansari MM, Dhasarathan P, Ranjitsingh AJA et al (2020) Ganoderma lucidum inspired silver nanoparticles and its biomedical applications with special reference to drug resistant Escherichia coli isolates from CAUTI. Saudi J Biol Sci 27:2993–3002
Alves-Barroco C, Rivas-Garcia L, Fernandes AR (2022) Light triggered enhancement of antibiotic efficacy in biofilm elimination mediated by gold-silver alloy nanoparticles. Front Microbiol 13:841124
Arslan M, Holyavkin C, Kisakesen HI et al (2018) Physiological and transcriptomic analysis of a chronologically long-lived Saccharomyces cerevisiae strain obtained by evolutionary engineering. Mol Biotechnol 60:468–484
Asiani KR, Williams H, Bird L et al (2016) SilE is an intrinsically disordered periplasmic “molecular sponge” involved in bacterial silver resistance. Mol Microbiol 101:731–742
Bai X, Nakatsu CH, Bhunia AK (2021) Bacterial biofilms and their implications in pathogenesis and food safety. Foods 10:2117
Balagna C, Perero S, Percivalle E et al (2020) Virucidal effect against coronavirus SARS-CoV-2 of a silver nanocluster/silica composite sputtered coating. Open Ceram 1:100006
Barros D, Pradhan A, Pascoal C, Cássio F (2021) Transcriptomics reveals the action mechanisms and cellular targets of citrate-coated silver nanoparticles in a ubiquitous aquatic fungus. Environ Pollut 268:115913
Barsyte D, Lovejoy DA, Lithgow GJ (2001) Longevity and heavy metal resistance in daf-2 and age-1 long-lived mutants of Caenorhabditis elegans. FASEB J 15:627–634
Bayat N, Rajapakse K, Marinsek-Logar R et al (2014) The effects of engineered nanoparticles on the cellular structure and growth of Saccharomyces cerevisiae. Nanotoxicology 8:363–373
Beneš V, Leonhardt T, Sácký J et al (2018) Two P(1B-1)-ATPases of Amanita strobiliformis with distinct properties in Ag/Cu transport. Front Microbiol 9:747
Çakar ZP, Turanlı-Yıldız B, Alkım C et al (2012) Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties. FEMS Yeast Res 12:171–182
Castro-Longoria E, Vilchis-Nestor AR, Avalos-Borja M (2011) Biosynthesis of silver, gold and bimetallic nanoparticles using the filamentous fungus Neurospora crassa. Colloids Surf B Biointerfaces 83:42–48
Chatterjee S, Ghosh R, Mandal NC (2020) Inhibition of biofilm- and hyphal- development, two virulent features of Candida albicans by secondary metabolites of an endophytic fungus Alternaria tenuissima having broad spectrum antifungal potential. Microbiol Res 232:126386
Chen JC, Lin ZH, Ma XX (2003) Evidence of the production of silver nanoparticles via pretreatment of Phoma sp.3.2883 with silver nitrate. Lett Appl Microbiol 37:105–108
Chopra I (2007) The increasing use of silver-based products as antimicrobial agents: a useful development or a cause for concern? J Antimicrob Chemother 59:587–590
Dal Co A, Brenner MP (2020) Tracing cell trajectories in a biofilm. Science 369:6499
Despax B, Saulou C, Raynaud P et al (2011) Transmission electron microscopy for elucidating the impact of silver-based treatments (ionic silver versus nanosilver-containing coating) on the model yeast Saccharomyces cerevisiae. Nanotechnology 22:175101
Durán N, Seabra AB, de Lima R (2014) Cytotoxicity and genotoxicity of biogenically synthesized silver nanoparticles. J Phys 1:245–263
Dutsch-Wicherek M, Sikora J, Tomaszewska R (2008) The possible biological role of metallothionein in apoptosis. Front Biosci 13:4029–4038
Edwards-Jones V (2009) The benefits of silver in hygiene, personal care and healthcare. Lett Appl Microbiol 49:147–152
El Sayed MT, El-Sayed ASA (2020) Tolerance and mycoremediation of silver ions by Fusarium solani. Heliyon 6:e03866
Elechiguerra JL, Burt JL, Morones JR et al (2005) Interaction of silver nanoparticles with HIV-1. J Nanobiotechnol 3:6
Foka FET, Mienie C, Bezuidenhout CC et al (2020) Complete genomic analysis of VRE from a cattle feedlot: Focus on 2 antibiotic resistance. Front Microbiol 11:571958
Gadanho M, Libkind D, Sampaio JP (2006) Yeast diversity in the extreme acidic environments of the Iberian Pyrite Belt. Microb Ecol 52:552–563
Galván Márquez I, Ghiyasvand M, Massarsky A et al (2018) Zinc oxide and silver nanoparticles toxicity in the baker’s yeast, Saccharomyces cerevisiae. PLoS ONE 13:e0193111
Gautam LK, Sharma P, Capalash N (2021) Attenuation of Acinetobacter baumannii virulence by inhibition of polyphosphate kinase 1 with repurposed drugs. Microbiol Res 242:126627
Gilmour MW, Thomson NR, Sanders M et al (2004) The complete nucleotide sequence of the resistance plasmid R478: defining the backbone components of incompatibility group H conjugative plasmids through comparative genomics. Plasmid 52:182–202
Graves JL Jr, Tajkarimi M, Cunningham Q et al (2015) Rapid evolution of silver nanoparticle resistance in Escherichia coli. Front Genet 6:42
Gugala N, Lemire J, Chatfield-Reed K et al (2018) Using a chemical genetic screen to enhance our understanding of the antibacterial properties of silver. Genes (Basel) 9:344
Gupta A, Phung LT, Taylor DE et al (2001) Diversity of silver resistance genes in IncH incompatibility group plasmids. Microbiol-SGM 147:3393–3402
Hamedi S, Ghaseminezhad M, Shokrollahzadeh S, Shojaosadati SA (2017) Controlled biosynthesis of silver nanoparticles using nitrate reductase enzyme induction of filamentous fungus and their antibacterial evaluation. Artif Cells Nanomedicine Biotechnol 45:1588–1596
Hamer DH (1986) Metallothionein. Annu Rev Biochem 55::913–951
Holland SL, Dyer PS, Bond CJ et al (2011) Candida argentea sp. nov., a copper and silver resistant yeast species. Fungal Biol 115:909–918
Horstmann C, Campbell C, Kim DS et al (2019) Transcriptome profile with 20 nm silver nanoparticles in yeast. FEMS Yeast Res 19:foz003
Hwang IS, Lee J, Hwang JH et al (2012) Silver nanoparticles induce apoptotic cell death in Candida albicans through the increase of hydroxyl radicals. FEBS J 279:1327–1338
Ikuma K, Decho AW, Lau BL (2015) When nanoparticles meet biofilms-interactions guiding the environmental fate and accumulation of nanoparticles. Front Microbiol 6:591
Jamshidinia N, Mohammadipanah F (2022) Nanomaterial-augmented formulation of disisnfectants and antiseptics in controlling SARS CoV-2. Food Environ Virol 14:105–119
Jeremiah SS, Miyakawa K, Morita T et al (2020) Potent antiviral effect of silver nanoparticles on SARS-CoV-2. Biochem Biophys Res Commun 533:195–200
Jian Y, Chen X, Ahmed T et al (2022) Toxicity and action mechanisms of silver nanoparticles against the mycotoxin-producing fungus Fusarium graminearum. J Adv Res 38:1–12
Jin YH, Dunlap PE, McBride SJ et al (2008) Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet 4:e1000053
Kanugala S, Kumar CG, Rachamalla HKR et al (2019) Chumacin-1 and Chumacin-2 from Pseudomonas aeruginosa strain CGK-KS-1 as novel quorum sensing signaling inhibitors for biocontrol of bacterial blight of rice. Microbiol Res 228:126301
Käosaar S, Kahru A, Mantecca P et al (2016) Profiling of the toxicity mechanisms of coated and uncoated silver nanoparticles to yeast Saccharomyces cerevisiae BY4741 using a set of its 9 single-gene deletion mutants defective in oxidative stress response, cell wall or membrane integrity and endocytosis. Toxicol In Vitro 35::149–162
Karygianni L, Ren Z, Koo H et al (2020) Biofilm Matrixome: Extracellular Components in Structured Microbial Communities. Trends Microbiol 28(8):668–681
Kasemets K, Käosaar S, Vija H et al (2019) Toxicity of differently sized and charged silver nanoparticles to yeast Saccharomyces cerevisiae BY4741: a nano-biointeraction perspective. Nanotoxicology 13:1041–1059
Khan I, Saeed K, Khan I (2019) Nanoparticles: Properties, applications and toxicities. Arab J Chem 12:908–931
Kim KJ, Sung WS, Suh BK et al (2009) Antifungal activity and mode of action of silver nano-particles on Candida albicans. Biometals 22:235–242
Kudrinskiy AA, Ivanov AY, Kulakovskaya EV et al (2014) The mode of action of silver and silver halides nanoparticles against Saccharomyces cerevisiae cells. J Nanoparticles 2014:568635
Kühlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5:282–295
Lara HH, Lopez-Ribot JL (2020) Inhibition of Mixed Biofilms of Candida albicans and Methicillin-Resistant Staphylococcus aureus by Positively Charged Silver Nanoparticles and Functionalized Silicone Elastomers. Pathogens 9:784
Lara HH, Garza-Treviño EN, Ixtepan-Turrent L et al (2011) Silver nanoparticles are broad-spectrum bactericidal and virucidal compounds. J Nanobiotechnol 9:30
Lara HH, Romero-Urbina DG, Pierce C et al (2015) Effect of silver nanoparticles on Candida albicans biofilms: an ultrastructural study. J Nanobiotechnol 13:91
Lee A-R, Lee S-J, Lee M et al (2017) A genome-wide screening of target genes against silver nanoparticles in fission yeast. Toxicol Sci 161:171–185
Lee B, Lee MJ, Yun SJ et al (2019) Silver nanoparticles induce reactive oxygen species-mediated cell cycle delay and synergistic cytotoxicity with 3-bromopyruvate in Candida albicans, but not in Saccharomyces cerevisiae. Int J Nanomedicine 14::4801–4816
Li Z, Cai Z, Cai Z et al (2020) Molecular genetic analysis of an XDR Pseudomonas aeruginosa ST664 clone carrying multiple conjugal plasmids. J Antimicrob Chemother 75:1443–1452
Lima de Silva AA, de Carvalho MA, de Souza SA et al (2012) Heavy metal tolerance (Cr, Ag AND Hg) in bacteria isolated from sewage. Braz J Microbiol 43:1620–1631
Liu M, Zhu X, Zhang C et al (2021) LuxQ-LuxU-LuxO pathway regulates biofilm formation by Vibrio parahaemolyticus. Microbiol Res 250:126791
Lok CN, Ho CM, Chen R et al (2008) Proteomic identification of the Cus system as a major determinant of constitutive Escherichia coli silver resistance of chromosomal origin. J Proteome Res 7:2351–2356
Madigan MT, Bender KS, Buckley DH et al (2019) Brock biology of microorganisms, Fifteenth edn. Pearson Education, Harlow, United Kingdom
Majeed S, Abdullah MS, bin, Dash GK et al (2016) Biochemical synthesis of silver nanoprticles using filamentous fungi Penicillium decumbens (MTCC-2494) and its efficacy against A-549 lung cancer cell line. Chin J Nat Med 14:615–620
Majeed S, Danish M, Binti Zahrudin AH, Dash GK (2018) Biosynthesis and characterization of silver nanoparticles from fungal species and its antibacterial and anticancer effect. Karbala Int J Mod Sci 4:86–92
Markowska K, Grudniak AM, Milczarek B et al (2018) The effect of silver nanoparticles on Listeria monocytogenes PCM2191 peptidoglycan metabolism and cell permeability. Pol J Microbiol 67:315–320
McQuillan JS, Infante HG, Stokes E et al (2012) Silver nanoparticle enhanced silver ion stress response in Escherichia coli K12. Nanotoxicology 6:857–866
Mehrbod P, Motamed N, Tabatabaian M et al (2009) In vitro antiviral effect of “Nanosilver” on influenza virus. DARU J Pharm Sci 17(2):88–93
Mijnendonckx K, Leys N, Mahillon J et al (2013) Antimicrobial silver: uses, toxicity and potential for resistance. Biometals 26:609–621
Monych NK, Turner RJ (2020) Multiple Compounds Secreted by Pseudomonas aeruginosa Increase the Tolerance of Staphylococcus aureus to the Antimicrobial Metals Copper and Silver. mSystems 5:e00746–20
Moreno A, Demitri N, Ruiz-Baca E et al (2019) Bioreduction of precious and heavy metals by Candida species under oxidative stress conditions. Microb Biotechnol 12:1164–1179
Muller M (2018) Bacterial Silver Resistance Gained by Cooperative Interspecies Redox Behavior. Antimicrob Agents Chemother 62:e00672–18
Muller M, Merrett ND (2014) Pyocyanin production by Pseudomonas aeruginosa confers resistance to ionic silver. Antimicrob Agents Chemother 58:5492–5499
Niazi JH, Sang BI, Kim YS et al (2011) Global gene response in Saccharomyces cerevisiae exposed to silver nanoparticles. Appl Biochem Biotechnol 164:1278–1291
Olasupo NA, Scott-Emuakpor MB, Ogunshola RA (1993) Resistance to heavy metals by some Nigerian yeast strains. Folia Microbiol (Praha) 38:285–287
Onyewu C, Blankenship JR, Del Poeta M et al (2003) Ergosterol biosynthesis inhibitors become fungicidal when combined with calcineurin inhibitors against Candida albicans, Candida glabrata, and Candida krusei. Antimicrob Agents Chemother 47:956–964
Ottoni CA, Simões MF, Fernandes S et al (2017) Screening of filamentous fungi for antimicrobial silver nanoparticles synthesis. AMB Express 7:31
Park HJ, Kim JY, Kim J et al (2009) Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. Water Res 43:1027–1032
Parmar P, Shukla A, Goswami D et al (2020) Comprehensive depiction of novel heavy metal tolerant and EPS producing bioluminescent Vibrio alginolyticus PBR1 and V. rotiferianus PBL1 confined from marine organisms. Microbiol Res 238:126526
Peixoto S, Loureiro S, Henriques I (2022) The impact of silver sulfide nanoparticles and silver ions in soil microbiome. J Hazard Mater 422:126793
Pereira L, Dias N, Carvalho J et al (2014) Synthesis, characterization and antifungal activity of chemically and fungal-produced silver nanoparticles against Trichophyton rubrum. J Appl Microbiol 117:1601–1613
Pümpel T, Schinner F (1986) Silver tolerance and silver accumulation of microorganisms from soil materials of a silver mine. Appl Microbiol Biotechnol 24:244–247
Qais FA, Shafiq A, Ahmad I et al (2020) Green synthesis of silver nanoparticles using Carum copticum: Assessment of its quorum sensing and biofilm inhibitory potential against gram negative bacterial pathogens. Microb Pathog 144:104172
Qin B, Fei C, Bridges AA et al (2020) Cell position fates and collective fountain flow in bacterial biofilms revealed by light-sheet microscopy. Science 369:71–77
Rad MR, Kirchrath L, Hollenberg CP (1994) A putative P-type Cu(2+)-transporting ATPase gene on chromosome II of Saccharomyces cerevisiae. Yeast 10:1217–1225
Radhakrishnan VS, Reddy Mudiam MK, Kumar M et al (2018) Silver nanoparticles induced alterations in multiple cellular targets, which are critical for drug susceptibilities and pathogenicity in fungal pathogen (Candida albicans). Int J Nanomedicine 13:2647–2663
Rai MK, Deshmukh SD, Ingle AP et al (2012) Silver nanoparticles: the powerful nanoweapon against multidrug-resistant bacteria. J Appl Microbiol 112:841–852
Randall CP, Oyama LB, Bostock JM et al (2013) The silver cation (Ag+): antistaphylococcal activity, mode of action and resistance studies. J Antimicrob Chemother 68:131–138
Randall CP, Gupta A, Jackson N et al (2015) Silver resistance in Gram-negative bacteria: a dissection of endogenous and exogenous mechanisms. J Antimicrob Chemother 70:1037–1046
Riggle PJ, Kumamoto CA (2000) Role of a Candida albicans P1-type ATPase in resistance to copper and silver ion toxicity. J Bacteriol 182:4899–4905
Robinson JR, Isikhuemhen OS, Anike FN (2021) Fungal–Metal Interactions: A Review of Toxicity and Homeostasis. J Fungi 7:225
Ruhal R, Kataria R (2021) Biofilm patterns in gram-positive and gram-negative bacteria. Microbiol Res 251:126829
Ruta LL, Banu MA, Neagoe AD et al (2018) Accumulation of Ag(I) by Saccharomyces cerevisiae cells expressing plant metallothioneins. Cells 7:266
Saeb ATM, Al-Rubeaan KA, Abouelhoda M et al (2017) Genome sequencing and analysis of the first spontaneous Nanosilver resistant bacterium Proteus mirabilis strain SCDR1. Antimicrob Resist Infect Control 6:119
Sanglard D, Ischer F, Marchetti O et al (2003) Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol Microbiol 48:959–976
Santos EMP, Martins CCB, Santos JVD et al (2021a) Silver nanoparticles-chitosan composites activity against resistant bacteria: tolerance and biofilm inhibition. J Nanoparticle Res 23:196
Santos TS, Silva TM, Cardoso JC et al (2021b) Biosynthesis of Silver Nanoparticles Mediated by Entomopathogenic Fungi: Antimicrobial Resistance, Nanopesticides, and Toxicity. Antibiotics 10:852
Sauer U (2001) Evolutionary engineering of industrially important microbial phenotypes. Adv Biochem Eng Biotechnol 73:130–166
Saulou C, Jamme F, Maranges C et al (2010) Synchrotron FTIR microspectroscopy of the yeast Saccharomyces cerevisiae after exposure to plasma-deposited nanosilver-containing coating. Anal Bioanal Chem 396::1441–1450
Saulou C, Jamme F, Girbal L et al (2013) Synchrotron FTIR microspectroscopy of Escherichia coli at single-cell scale under silver-induced stress conditions. Anal Bioanal Chem 405::2685–2697
Selvaraj A, Valliammai A, Premika M et al (2021) Sapindus mukorossi Gaertn. and its bioactive metabolite oleic acid impedes methicillin-resistant Staphylococcus aureus biofilm formation by down regulating adhesion genes expression. Microbiol Res 242:126601
Şen M, Yılmaz U, Baysal A et al (2011) In vivo evolutionary engineering of a boron-resistant bacterium: Bacillus boroniphilus. Antonie Van Leeuwenhoek 99:825–835
Shukla A, Parmar P, Patel B et al (2021) Breaking bad: Better call gingerol for improving antibiotic susceptibility of Pseudomonas aeruginosa by inhibiting multiple quorum sensing pathways. Microbiol Res 252:126863
Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341–353
Silver S, Phung le T, Silver G (2006) Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J Ind Microbiol Biotechnol 33:627–634
Singhal RK, Anderson ME, Meister A (1987) Glutathione, a first line of defense against cadmium toxicity. FASEB J 1:220–223
Solioz M, Odermatt A (1995) Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J Biol Chem 270:9217–9221
Solioz M, Vulpe C (1996) CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21:237–241
Sportelli MC, Izzi M, Kukushkina EA et al (2020) Can nanotechnology and materials science help the fight against SARS-CoV-2? Nanomaterials. (Basel Switzerland) 10:802
Staehlin BM, Gibbons JG, Rokas A et al (2016) Evolution of a heavy metal homeostasis/resistance island reflects increasing copper stress in enterobacteria. Genome Biol Evol 8:811–826
Sudheer Khan S, Bharath Kumar E, Mukherjee A et al (2011) Bacterial tolerance to silver nanoparticles (SNPs): Aeromonas punctata isolated from sewage environment. J Basic Microbiol 51::183–190
Sultan I, Ali A, Gogry FA et al (2020) Bacterial isolates harboring antibiotics and heavy-metal resistance genes co-existing with mobile genetic elements in natural aquatic water bodies. Saudi J Biol Sci 27:2660–2668
Taff HT, Nett JE, Zarnowski R et al (2012) A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathog 8:e1002848
Terzioğlu E, Alkım C, Arslan M et al (2020) Genomic, transcriptomic and physiological analyses of silver-resistant Saccharomyces cerevisiae obtained by evolutionary engineering. Yeast 37:413–426
Trefry JC (2011) The development of silver nanoparticles as antiviral agents. Doctoral dissertation, Wright State University
Trefry JC, Wooley DP (2012) Rapid assessment of antiviral activity and cytotoxicity of silver nanoparticles using a novel application of the tetrazolium-based colorimetric assay. J Virol Methods 183:19–24
Vagabov VM, Ivanov AY, Kulakovskaya TV et al (2008) Efflux of potassium ions from cells and spheroplasts of Saccharomyces cerevisiae yeast treated with silver and copper ions. Biochem (Mosc) 73:1224–1227
Vazquez-Munoz R, Lopez-Ribot JL (2020) Nanotechnology as an Alternative to Reduce the Spread of COVID-19. Challenges 11:15
Vazquez-Muñoz R, Avalos-Borja M, Castro-Longoria E (2014) Ultrastructural analysis of Candida albicans when exposed to silver nanoparticles. PLoS ONE 9:e108876
Vest KE, Leary SC, Winge DR et al (2013) Copper import into the mitochondrial matrix in Saccharomyces cerevisiae is mediated by Pic2, a mitochondrial carrier family protein. J Biol Chem 288:23884–23892
Völlmecke C, Drees SL, Reimann J et al (2012) The ATPases CopA and CopB both contribute to copper resistance of the thermoacidophilic archaeon Sulfolobus solfataricus. Microbiol-SGM 158:1622–1633
Wang X, Cheng Y, Zhang W et al (2021) (p)ppGpp synthetases are required for the pathogenicity of Salmonella Pullorum in chickens. Microbiol Res 245:126685
Wei MP, Yu H, Gou YH et al (2022) Synergistic combination of Sapindoside A and B: A novel antibiofilm agent against Cutibacterium acnes. Microbiol Res 254:126912
Xie JL (2017) Stress response pathways regulate drug resistance and morphogenesis in the human fungal pathogen Candida albicans. Doctoral dissertation, University of Toronto
Yang HC, Pon LA (2003) Toxicity of metal ions used in dental alloys: a study in the yeast Saccharomyces cerevisiae. Drug Chem Toxicol 26:75–85
Yazgan A, Özcengiz G (1994) Subcellular distribution of accumulated heavy metals in Saccharomyces cerevisiae and Kluyveromyces marxianus. Biotechnol Lett 16:871–874
Yazgan A, Ozcengiz G, Alaeddinoglu NG (1993) Studies on metal resistance system in Kluyveromyces marxianus. Biol Trace Elem Res 38:117–127
Yuan DS, Stearman R, Dancis A et al (1995) The Menkes/Wilson disease gene homologue in yeast provides copper to a ceruloplasmin-like oxidase required for iron uptake. Proc Natl Acad Sci U S A 92:2632–2636
Zhang Y, Pan X, Liao S et al (2020) Quantitative Proteomics Reveals the Mechanism of Silver Nanoparticles against Multidrug-Resistant Pseudomonas aeruginosa Biofilms. J Proteome Res 19:3109–3122
Zhang N, Zhang S, Ren W et al (2021a) Roles of rpoN in biofilm formation of Vibrio alginolyticus HN08155 at different cell densities. Microbiol Res 247:126728
Zhang X, Dang D, Zheng LS et al (2021b) Effect of Ag nanoparticles on denitrification and microbial community in a paddy soil. Front Microbiol 12:785439
Zhang Y, Qi J, Wang Y et al (2022) Comparative study of the role of surfactin-triggered signaling in biofilm formation among different Bacillus species. Microbiol Res 254:126920
Zimmermann M, Udagedara SR, Sze CM et al (2012) PcoE–a metal sponge expressed to the periplasm of copper resistance Escherichia coli. Implication of its function role in copper resistance. J Inorg Biochem 115:186–197
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This review paper is dedicated to the memory of Prof. Dr. Fatma Neşe Kök, our beloved Head of the Department of Molecular Biology and Genetics, Istanbul Technical University (ITU), and Director of Dr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), who passed away while this paper was under revision.
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ZPÇ prepared the outline for the manuscript. ET, MA, BGB and ZPÇ wrote the main manuscript text. ZPÇ revised the manuscript. ET and MA prepared Figures 1-3. ET prepared the Graphical Abstract. All authors reviewed the manuscript.
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Ergi Terzioğlu and Mevlüt Arslan have contributed equally to this work.
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Terzioğlu, E., Arslan, M., Balaban, B.G. et al. Microbial silver resistance mechanisms: recent developments. World J Microbiol Biotechnol 38, 158 (2022). https://doi.org/10.1007/s11274-022-03341-1
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DOI: https://doi.org/10.1007/s11274-022-03341-1