Zinc effects on bacteria: insights from Escherichia coli by multi-omics approach
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.2.69/0.0/0.0/19_073/0016670
EC | EU Social | European Social Fund (ESF)
CZ.02.2.69/0.0/0.0/19_073/0016670
EC | EU Social | European Social Fund (ESF)
CZ.02.2.69/0.0/0.0/19_073/0016670
EC | EU Social | European Social Fund (ESF)
CZ.02.2.69/0.0/0.0/19_073/0016670
EC | EU Social | European Social Fund (ESF)
CZ.02.2.69/0.0/0.0/19_073/0016670
EC | EU Social | European Social Fund (ESF)
PubMed
37905937
PubMed Central
PMC10734530
DOI
10.1128/msystems.00733-23
Knihovny.cz E-zdroje
- Klíčová slova
- antimicrobial resistance, genome, nanoparticles, phenotype, proteome, transcriptome, virulence, zinc, zinc oxide,
- MeSH
- Escherichia coli genetika MeSH
- lidé MeSH
- multiomika MeSH
- oxid zinečnatý * chemie MeSH
- proteomika MeSH
- zinek * farmakologie MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- oxid zinečnatý * MeSH
- zinek * MeSH
A long-term exposure of bacteria to zinc oxide and zinc oxide nanoparticles leads to major alterations in bacterial morphology and physiology. These included biochemical and physiological processes promoting the emergence of strains with multi-drug resistance and virulence traits. After the removal of zinc pressure, bacterial phenotype reversed back to the original state; however, certain changes at the genomic, transcriptomic, and proteomic level remained. Why is this important? The extensive and intensive use of supplements in animal feed effects the intestinal microbiota of livestock and this may negatively impact the health of animals and people. Therefore, it is crucial to understand and monitor the impact of feed supplements on intestinal microorganisms in order to adequately assess and prevent potential health risks.
Central European Institute of Technology University of Veterinary Sciences Brno Brno Czechia
Faculty of Horticulture Mendeleum Institute of Genetics Mendel University in Brno Brno Czechia
Faculty of Medicine in Pilsen Biomedical Center Charles University Pilsen Czechia
Zobrazit více v PubMed
Ali H, Khan E. 2017. Environmental chemistry in the twenty-first century. Environ Chem Lett 15:329–346. doi:10.1007/s10311-016-0601-3 DOI
Zhou YT, Wang LL, Xiao TF, Chen YH, Beiyuan JZ, She JY, Zhou YC, Yin ML, Liu J, Liu YY, Wang YX, Wang J. 2020. Legacy of multiple heavy metal(loid)s contamination and ecological risks in farmland soils from a historical artisanal zinc smelting area. Sci Total Environ 720:137541. doi:10.1016/j.scitotenv.2020.137541 PubMed DOI
García-Gómez C, García-Gutiérrez S, Obrador A, Fernández MD. 2020. Study of Zn availability, uptake, and effects on earthworms of zinc oxide nanoparticle versus bulk applied to two agricultural soils: acidic and calcareous. Chemosphere 239:124814. doi:10.1016/j.chemosphere.2019.124814 PubMed DOI
Shi TR, Ma J, Wu X, Ju TA, Lin XL, Zhang YY, Li XH, Gong YW, Hou H, Zhao L, Wu FY. 2018. Inventories of heavy metal inputs and outputs to and from agricultural soils: a review. Ecotoxicol Environ Saf 164:118–124. doi:10.1016/j.ecoenv.2018.08.016 PubMed DOI
Dębski B. 2016. Supplementation of pigs diet with zinc and copper as alternative to conventional antimicrobials. Pol J Vet Sci 19:917–924. doi:10.1515/pjvs-2016-0113 PubMed DOI
Schlegel P, Nys Y, Jondreville C. 2010. Zinc availability and digestive zinc solubility in piglets and broilers fed diets varying in their phytate contents, phytase activity and supplemented zinc source. Animal 4:200–209. doi:10.1017/S1751731109990978 PubMed DOI
EPo A, PoSuiA F. 2014. Scientific opinion on the potential reduction of the currently authorised maximum zinc content in complete feed. EFS2 12:3668. doi:10.2903/j.efsa.2014.3668 DOI
Flavourings AP. 2016. Safety assessment of the substance zinc oxide, nanoparticles, for use in food contact materials. EFS2 14:4408. doi:10.2903/j.efsa.2016.4408 DOI
Aquilina G, Bampidis V, Bastos MD, Costa LG, Flachowsky G, Gralak MA, Hogstrand C, Leng L, Lopez-Puente S, Martelli G, Mayo B, Ramos F, Renshaw D, Rychen G, Saarela M, Sejrsen K, Beelen P, Wallace RJ, Westendorf J, EPAPS A. 2014. Scientific opinion on the potential reduction of the currently authorised maximum zinc content in complete feed. EFS2 12. doi:10.2903/j.efsa.2014.3668 DOI
García-Gómez C, Obrador A, González D, Babín M, Fernández MD. 2017. Comparative effect of ZnO NPs, ZnO bulk and ZnSO4 in the antioxidant defences of two plant species growing in two agricultural soils under greenhouse conditions. Sci Total Environ 589:11–24. doi:10.1016/j.scitotenv.2017.02.153 PubMed DOI
Vats P, Kaur UJ, Rishi P. 2022. Heavy metal-induced selection and proliferation of antibiotic resistance: a review. J Appl Microbiol 132:4058–4076. doi:10.1111/jam.15492 PubMed DOI
Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D, Andersson DI. 2011. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7:e1002158. doi:10.1371/journal.ppat.1002158 PubMed DOI PMC
Gullberg E, Albrecht LM, Karlsson C, Sandegren L, Andersson DI. 2014. Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. mBio 5:e01918-14. doi:10.1128/mBio.01918-14 PubMed DOI PMC
Guðmundsdóttir JS, Fredheim EGA, Koumans CIM, Hegstad J, Tang P-C, Andersson DI, Samuelsen Ø, Johnsen PJ. 2021. The chemotherapeutic drug methotrexate selects for antibiotic resistance. EBioMedicine 74:103742. doi:10.1016/j.ebiom.2021.103742 PubMed DOI PMC
Wu T, Gagnon A, McGourty K, DosSantos R, Chanetsa L, Zhang BC, Bello D, Kelleher SL. 2021. Zinc exposure promotes commensal-to-pathogen transition in Pseudomonas aeruginosa leading to mucosal inflammation and illness in mice. Int J Mol Sci 22:13321. doi:10.3390/ijms222413321 PubMed DOI PMC
Li XY, Gu AZ, Zhang Y, Xie B, Li D, Chen JM. 2019. Sub-lethal concentrations of heavy metals induce antibiotic resistance via mutagenesis. J Hazard Mater 369:9–16. doi:10.1016/j.jhazmat.2019.02.006 PubMed DOI
Oz T, Guvenek A, Yildiz S, Karaboga E, Tamer YT, Mumcuyan N, Ozan VB, Senturk GH, Cokol M, Yeh P, Toprak E. 2014. Strength of selection pressure is an important parameter contributing to the complexity of antibiotic resistance evolution. Mol Biol Evol 31:2387–2401. doi:10.1093/molbev/msu191 PubMed DOI PMC
Johnsen PJ, Townsend JP, Bøhn T, Simonsen GS, Sundsfjord A, Nielsen KM. 2009. Factors affecting the reversal of antimicrobial-drug resistance. Lancet Infect Dis 9:357–364. doi:10.1016/S1473-3099(09)70105-7 PubMed DOI
Dickinson AW, Power A, Hansen MG, Brandt KK, Piliposian G, Appleby P, O’Neill PA, Jones RT, Sierocinski P, Koskella B, Vos M. 2019. Heavy metal pollution and co-selection for antibiotic resistance: a microbial palaeontology approach. Environ Int 132:105117. doi:10.1016/j.envint.2019.105117 PubMed DOI
Peltier E, Vincent J, Finn C, Graham DW. 2010. Zinc-induced antibiotic resistance in activated sludge bioreactors. Water Res. 44:3829–3836. doi:10.1016/j.watres.2010.04.041 PubMed DOI
Ziebuhr W, Hennig S, Eckart M, Kränzler H, Batzilla C, Kozitskaya S. 2006. Nosocomial infections by Staphylococcus epidermidis: how a commensal bacterium turns into a pathogen. Int J Antimicrob Agents 28 Suppl 1:S14–S20. doi:10.1016/j.ijantimicag.2006.05.012 PubMed DOI
Matyszczuk K, Krzepiłko A. 2022. Model study for interaction of sublethal doses of zinc oxide nanoparticles with environmentally beneficial bacteria Bacillus thuringiensis and Bacillus megaterium Int J Mol Sci 23:11820. doi:10.3390/ijms231911820 PubMed DOI PMC
Murray SA, Amachawadi RG, Norman KN, Lawhon SD, Nagaraja TG, Drouillard JS, Scott HM. 2021. Effects of zinc and menthol-based diets on co-selection of antibiotic resistance among E. coli and Enterococcus spp. In beef cattle. Animals (Basel) 11:259. doi:10.3390/ani11020259 PubMed DOI PMC
Li H, Xu H, Song HL, Lu Y, Yang XL. 2020. Antibiotic resistance genes, bacterial communities, and functions in constructed wetland-microbial fuel cells: responses to the co-stresses of antibiotics and zinc. Environ Pollut 265:115084. doi:10.1016/j.envpol.2020.115084 PubMed DOI
Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, Brennan RG. 2009. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 323:396–401. doi:10.1126/science.1163806 PubMed DOI PMC
Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DGJ. 2015. Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 16:964. doi:10.1186/s12864-015-2153-5 PubMed DOI PMC
Imran M, Das KR, Naik MM. 2019. Co-selection of multi-antibiotic resistance in bacterial pathogens in metal and microplastic contaminated environments: an emerging health threat. Chemosphere 215:846–857. doi:10.1016/j.chemosphere.2018.10.114 PubMed DOI
Brayner R, Ferrari-Iliou R, Brivois N, Djediat S, Benedetti MF, Fiévet F. 2006. Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett. 6:866–870. doi:10.1021/nl052326h PubMed DOI
Jones N, Ray B, Ranjit KT, Manna AC. 2008. Antibacterial activity of ZnO nanoparticle suspensions on a broad spectrum of microorganisms. FEMS Microbiol Lett 279:71–76. doi:10.1111/j.1574-6968.2007.01012.x PubMed DOI
Anonymous . 2023. Testing, E.C.O.A.S., Breakpoint tables for interpretation of Mics and zone diameters. 2023, version
Brown LR, Caulkins RC, Schartel TE, Rosch JW, Honsa ES, Schultz-Cherry S, Meliopoulos VA, Cherry S, Thornton JA. 2017. Increased zinc availability enhances initial aggregation and Biofilm formation of Streptococcus pneumoniae Front Cell Infect Microbiol 7:233. doi:10.3389/fcimb.2017.00233 PubMed DOI PMC
Das S, Dash HR, Chakraborty J. 2016. Genetic basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants. Appl Microbiol Biotechnol 100:2967–2984. doi:10.1007/s00253-016-7364-4 PubMed DOI
Hall AR. 2013. Genotype-by-environment interactions due to antibiotic resistance and adaptation in Escherichia coli. J Evol Biol 26:1655–1664. doi:10.1111/jeb.12172 PubMed DOI
Johanns VC, Epping L, Semmler T, Ghazisaeedi F, Lübke-Becker A, Pfeifer Y, Eichhorn I, Merle R, Bethe A, Walther B, Wieler LH. 2020. High-zinc supplementation of weaned piglets affects frequencies of virulence and bacteriocin associated genes among intestinal Escherichia coli populations. Front Vet Sci 7:614513. doi:10.3389/fvets.2020.614513 PubMed DOI PMC
Kociova S, Dolezelikova K, Horky P, Skalickova S, Baholet D, Bozdechova L, Vaclavkova E, Belkova J, Nevrkla P, Skladanka J, Do T, Zitka O, Haddad Y, Kopel P, Zurek L, Adam V, Smerkova K. 2020. Zinc phosphate-based nanoparticles as alternatives to zinc oxide in diet of weaned piglets. J Anim Sci Biotechnol 11:59. doi:10.1186/s40104-020-00458-x PubMed DOI PMC
Wales AD, Davies RH. 2015. Co-selection of resistance to antibiotics, biocides and heavy metals, and its relevance to foodborne pathogens. Antibiotics (Basel) 4:567–604. doi:10.3390/antibiotics4040567 PubMed DOI PMC
Krause KM, Serio AW, Kane TR, Connolly LE. 2016. Aminoglycosides: an overview. Cold Spring Harb Perspect Med 6:a027029. doi:10.1101/cshperspect.a027029 PubMed DOI PMC
Poole K. 2007. Efflux pumps as antimicrobial resistance mechanisms. Ann Med 39:162–176. doi:10.1080/07853890701195262 PubMed DOI
Ibacache-Quiroga C, Oliveros JC, Couce A, Blázquez J. 2018. Parallel evolution of high-level aminoglycoside resistance in Escherichia coli under low and high mutation supply rates. Front Microbiol 9:427. doi:10.3389/fmicb.2018.00427 PubMed DOI PMC
Scheunemann AE, Graham WD, Vendeix FAP, Agris PF. 2010. Binding of aminoglycoside antibiotics to helix 69 of 23S rRNA. Nucleic Acids Res 38:3094–3105. doi:10.1093/nar/gkp1253 PubMed DOI PMC
McCoy LS, Xie Y, Tor Y. 2011. Antibiotics that target protein synthesis. Wiley Interdiscip Rev RNA 2:209–232. doi:10.1002/wrna.60 PubMed DOI
McCollister BD, Hoffman M, Husain M, Vázquez-Torres A. 2011. Nitric oxide protects bacteria from aminoglycosides by blocking the energy-dependent phases of drug uptake. Antimicrob Agents Chemother 55:2189–2196. doi:10.1128/AAC.01203-10 PubMed DOI PMC
Jacoby GA. 2009. AmpC β-lactamases. Clin Microbiol Rev 22:161–182. doi:10.1128/CMR.00036-08 PubMed DOI PMC
Nagano K, Nikaido H. 2009. Kinetic behavior of the major multidrug efflux pump AcrB of Escherichia coli. Proc Natl Acad Sci U S A 106:5854–5858. doi:10.1073/pnas.0901695106 PubMed DOI PMC
Mohiuddin SG, Massahi A, Orman MA, Khursigara CM. 2022. High-throughput screening of a promoter library reveals new persister mechanisms in Escherichia coli. Microbiol Spectr 10:e0225321. doi:10.1128/spectrum.02253-21 PubMed DOI PMC
Han XL, Dorsey-Oresto A, Malik M, Wang JY, Drlica K, Zhao XL, Lu T. 2010. Escherichia coli genes that reduce the lethal effects of stress. BMC Microbiol 10:35. doi:10.1186/1471-2180-10-35 PubMed DOI PMC
Pasqua M, Bonaccorsi di Patti MC, Fanelli G, Utsumi R, Eguchi Y, Trirocco R, Prosseda G, Grossi M, Colonna B. 2021. Host - bacterial pathogen communication: the wily role of the multidrug efflux pumps of the MFS family. Front Mol Biosci 8:723274. doi:10.3389/fmolb.2021.723274 PubMed DOI PMC
Pu YY, Ke YH, Bai F. 2017. Active efflux in dormant bacterial cells - new insights into antibiotic persistence. Drug Resist Updat 30:7–14. doi:10.1016/j.drup.2016.11.002 PubMed DOI
Wan Y, Wang M, Chan EWC, Chen S, Khursigara CM. 2021. Membrane transporters of the major facilitator superfamily are essential for long-term maintenance of phenotypic tolerance to multiple antibiotics in E. coli. Microbiol Spectr 9:e0184621. doi:10.1128/Spectrum.01846-21 PubMed DOI PMC
Suryawati B. 2018. Zinc homeostasis mechanism and its role in bacterial virulence capacity. AIP Conf Proc. doi:10.1063/1.5062819 DOI
Wüthrich D, Brilhante M, Hausherr A, Becker J, Meylan M, Perreten V. 2019. A novel trimethoprim resistance gene, dfrA36, characterized from Escherichia coli from calves. mSphere 4:e00255-19. doi:10.1128/mSphere.00255-19 PubMed DOI PMC
Shi HM, Li T, Xu JT, Yu JF, Yang SS, Zhang XE, Tao SC, Gu J, Deng JY. 2021. MgrB inactivation confers Trimethoprim resistance in Escherichia coli. Front Microbiol 12:682205. doi:10.3389/fmicb.2021.682205 PubMed DOI PMC
Schwarz S, Kehrenberg C, Doublet B, Cloeckaert A. 2004. Molecular basis of bacterial resistance to chloramphenicol and florfenicol. FEMS Microbiol Rev 28:519–542. doi:10.1016/j.femsre.2004.04.001 PubMed DOI
Montero CI, Johnson MR, Chou CJ, Conners SB, Geouge SG, Tachdjian S, Nichols JD, Kelly RM. 2007. Responses of wild-type and resistant strains of the hyperthermophilic bacterium thermotoga maritima to chloramphenicol challenge. Appl Environ Microbiol 73:5058–5065. doi:10.1128/AEM.00453-07 PubMed DOI PMC
Daniels C, Ramos JL. 2009. Adaptive drug resistance mediated by root-nodulation-cell division efflux pumps. Clin Microbiol Infect 15 Suppl 1:32–36. doi:10.1111/j.1469-0691.2008.02693.x PubMed DOI
Cui HL, Smith AL. 2022. Impact of engineered nanoparticles on the fate of antibiotic resistance genes in wastewater and receiving environments: a comprehensive review. Environ Res 204:112373. doi:10.1016/j.envres.2021.112373 PubMed DOI
Lin TY, Santos TMA, Kontur WS, Donohue TJ, Weibel DB. 2015. A cardiolipin-deficient mutant of rhodobacter sphaeroides has an altered cell shape and is impaired in Biofilm formation. J Bacteriol 197:3446–3455. doi:10.1128/JB.00420-15 PubMed DOI PMC
van Teeseling MCF, de Pedro MA, Cava F. 2017. Determinants of bacterial morphology: from fundamentals to possibilities for antimicrobial targeting. Front Microbiol 8:1264. doi:10.3389/fmicb.2017.01264 PubMed DOI PMC
Morè N, Martorana AM, Biboy J, Otten C, Winkle M, Serrano CKG, Montón Silva A, Atkinson L, Yau H, Breukink E, den Blaauwen T, Vollmer W, Polissi A. 2019. Peptidoglycan remodeling enables Escherichia coli to survive severe outer membrane assembly defect. mBio 10:e02729-18. doi:10.1128/mBio.02729-18 PubMed DOI PMC
Nikaido H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656. doi:10.1128/MMBR.67.4.593-656.2003 PubMed DOI PMC
Hugonnet J-E, Mengin-Lecreulx D, Monton A, den Blaauwen T, Carbonnelle E, Veckerlé C, Brun YV, van Nieuwenhze M, Bouchier C, Tu K, Rice LB, Arthur M. 2016. Factors essential for L,D-transpeptidase-mediated peptidoglycan cross-linking and beta-lactam resistance in Escherichia coli Elife 5:e19469. doi:10.7554/eLife.19469 PubMed DOI PMC
Li XJ, Xue X, Jia J, Zou XC, Guan YJ, Zhu L, Wang ZZ. 2023. Nonsteroidal anti-inflammatory drug diclofenac accelerates the emergence of antibiotic resistance via mutagenesis. Environmental Pollution 326:121457. doi:10.1016/j.envpol.2023.121457 PubMed DOI
Lee M, Hesek D, Llarrull LI, Lastochkin E, Pi HL, Boggess B, Mobashery S. 2013. Reactions of all Escherichia coli lytic transglycosylases with bacterial cell wall. J Am Chem Soc 135:3311–3314. doi:10.1021/ja309036q PubMed DOI PMC
Domínguez-Gil T, Molina R, Alcorlo M, Hermoso JA. 2016. Renew or die: the molecular mechanisms of peptidoglycan recycling and antibiotic resistance in gram-negative pathogens. Drug Resist Updat 28:91–104. doi:10.1016/j.drup.2016.07.002 PubMed DOI
Prüss BM, Besemann C, Denton A, Wolfe AJ. 2006. A complex transcription network controls the early stages of biofilm development by Escherichia coli. J Bacteriol 188:3731–3739. doi:10.1128/JB.01780-05 PubMed DOI PMC
Li J, Attila C, Wang L, Wood TK, Valdes JJ, Bentley WE. 2007. Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture. J Bacteriol 189:6011–6020. doi:10.1128/JB.00014-07 PubMed DOI PMC
May T, Okabe S. 2011. Enterobactin is required for biofilm development in reduced-genome Escherichia coli. Environ Microbiol 13:3149–3162. doi:10.1111/j.1462-2920.2011.02607.x PubMed DOI
Tuckerman JR, Gonzalez G, Gilles-Gonzalez M-A. 2011. Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407:633–639. doi:10.1016/j.jmb.2011.02.019 PubMed DOI
Méndez-Ortiz MM, Hyodo M, Hayakawa Y, Membrillo-Hernández J. 2006. Genome-wide transcriptional profile of Escherichia coli in response to high levels of the second messenger 3 ',5 '-cyclic diguanylic acid. J Biol Chem 281:8090–8099. doi:10.1074/jbc.M510701200 PubMed DOI
Domka J, Lee JT, Bansal T, Wood TK. 2007. Temporal gene-expression in Escherichia coli K-12 biofilms. Environ Microbiol 9:332–346. doi:10.1111/j.1462-2920.2006.01143.x PubMed DOI
Singer HM, Erhardt M, Hughes KT. 2014. Comparative analysis of the secretion capability of early and late flagellar type III secretion substrates. Mol Microbiol 93:505–520. doi:10.1111/mmi.12675 PubMed DOI PMC
Chellappa ST, Maredia R, Phipps K, Haskins WE, Weitao T. 2013. Motility of Pseudomonas aeruginosa contributes to SOS-inducible biofilm formation. Res Microbiol 164:1019–1027. doi:10.1016/j.resmic.2013.10.001 PubMed DOI
Pena RT, Blasco L, Ambroa A, González-Pedrajo B, Fernández-García L, López M, Bleriot I, Bou G, García-Contreras R, Wood TK, Tomás M. 2019. Relationship between quorum sensing and secretion systems. Front Microbiol 10:1100. doi:10.3389/fmicb.2019.01100 PubMed DOI PMC
Neuer A, Spandorfer SD, Giraldo P, Dieterle S, Rosenwaks Z, Witkin SS. 2000. The role of heat shock proteins in reproduction. Hum Reprod Update 6:149–159. doi:10.1093/humupd/6.2.149 PubMed DOI
Siddiqi KS, Ur Rahman ATajuddinHusen A. 2018. Properties of zinc oxide nanoparticles and their activity against microbes. Nanoscale Res Lett 13:141. doi:10.1186/s11671-018-2532-3 PubMed DOI PMC
Marietou A, Nguyen ATT, Allen EE, Bartlett DH. 2014. Adaptive laboratory evolution of Escherichia coli K-12 MG1655 for growth at high hydrostatic pressure. Front Microbiol 5:749. doi:10.3389/fmicb.2014.00749 PubMed DOI PMC
Sangpuii L, Dixit SK, Kumawat M, Apoorva S, Kumar M, Kappala D, Goswami TK, Mahawar M. 2018. Comparative roles of clpA and clpB in the survival of S. typhimurium under stress and virulence in poultry. Sci Rep 8:4481. doi:10.1038/s41598-018-22670-6 PubMed DOI PMC
Dougan DA, Reid BG, Horwich AL, Bukau B. 2002. ClpS, a substrate modulator of the ClpAP machine. Mol Cell 9:673–683. doi:10.1016/s1097-2765(02)00485-9 PubMed DOI
Bradley MD, Beach MB, de Koning APJ, Pratt TS, Osuna R. 2007. Effects of fis on Escherichia coli gene expression during different growth stages. Microbiology 153:2922–2940. doi:10.1099/mic.0.2007/008565-0 PubMed DOI
Ilbert M, Horst J, Ahrens S, Winter J, Graf PCF, Lilie H, Jakob U. 2007. The redox-switch domain of Hsp33 functions as dual stress sensor. Nat Struct Mol Biol 14:556–563. doi:10.1038/nsmb1244 PubMed DOI PMC
Itoh Y, Wang X, Hinnebusch BJ, Preston JF, Romeo T. 2005. Depolymerization of β-1, 6-N-acetyl-D-glucosamine disrupts the integrity of diverse bacterial biofilms. J Bacteriol 187:382–387. doi:10.1128/JB.187.1.382-387.2005 PubMed DOI PMC
Morè N, Martorana AM, Biboy J, Otten C, Winkle M, Serrano CKG, Montón Silva A, Atkinson L, Yau H, Breukink E, den Blaauwen T, Vollmer W, Polissi A. 2019. Peptidoglycan remodeling enables Escherichia coli to survive severe outer membrane assembly defect. mBio 10:e02729-18. doi:10.1128/mBio.02729-18 PubMed DOI PMC
Rhee J-S, Raisuddin S, Lee K-W, Seo JS, Ki J-S, Kim I-C, Park HG, Lee J-S. 2009. Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp Biochem Physiol C Toxicol Pharmacol 149:104–112. doi:10.1016/j.cbpc.2008.07.009 PubMed DOI
Chuang SE, Blattner FR. 1993. Characterization of 26 new heat-shock genes of Escherichia coli. J Bacteriol 175:5242–5252. doi:10.1128/jb.175.16.5242-5252.1993 PubMed DOI PMC
Kohanski MA, DePristo MA, Collins JJ. 2010. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol Cell 37:311–320. doi:10.1016/j.molcel.2010.01.003 PubMed DOI PMC
Orban K, Finkel SE. 2022. Dps is a universally conserved dual-action DNA-binding and ferritin protein. J Bacteriol 204:e0003622. doi:10.1128/jb.00036-22 PubMed DOI PMC
Knorr S, Sinn M, Galetskiy D, Williams RM, Wang C, Müller N, Mayans O, Schleheck D, Hartig JS. 2018. Widespread bacterial lysine degradation proceeding via glutarate and L-2-hydroxyglutarate. Nat Commun 9:5071. doi:10.1038/s41467-018-07563-6 PubMed DOI PMC
Glebes TY, Sandoval NR, Gillis JH, Gill RT. 2015. Comparison of genome-wide selection strategies to identify furfural tolerance genes in Escherichia coli . Biotechnol. Bioeng. 112:129–140. doi:10.1002/bit.25325 PubMed DOI
Ceci P, Di Cecca G, Falconi M, Oteri F, Zamparelli C, Chiancone E. 2011. Effect of the charge distribution along the "ferritin-like" pores of the proteins from the Dps family on the iron incorporation process. J Biol Inorg Chem 16:869–880. doi:10.1007/s00775-011-0784-9 PubMed DOI
Figueira R, Brown DR, Ferreira D, Eldridge MJG, Burchell L, Pan ZS, Helaine S, Wigneshweraraj S. 2015. Adaptation to sustained nitrogen starvation by Escherichia coli requires the eukaryote-like serine/threonine kinase YeaG. Sci Rep 5:17524. doi:10.1038/srep17524 PubMed DOI PMC
Jeje O, Ewunkem AJ, Jeffers-Francis LK, Graves JL. 2023. Serving two masters: effect of Escherichia coli dual resistance on antibiotic susceptibility. Antibiotics (Basel) 12:603. doi:10.3390/antibiotics12030603 PubMed DOI PMC
Yoshida H, Maki Y, Furuike S, Sakai A, Ueta M, Wada A. 2012. YqjD is an inner membrane protein associated with stationary-phase ribosomes in Escherichia coli. J Bacteriol 194:4178–4183. doi:10.1128/JB.00396-12 PubMed DOI PMC
Geisel N, Vilar JMG, Rubi JM. 2011. Optimal resting-growth strategies of microbial populations in fluctuating environments. PLoS One 6:e18622. doi:10.1371/journal.pone.0018622 PubMed DOI PMC
Lam O, Wheeler J, Tang CM. 2014. Thermal control of virulence factors in bacteria: a hot topic. Virulence 5:852–862. doi:10.4161/21505594.2014.970949 PubMed DOI PMC
Panáček A, Kvítek L, Smékalová M, Večeřová R, Kolář M, Röderová M, Dyčka F, Šebela M, Prucek R, Tomanec O, Zbořil R. 2018. Bacterial resistance to silver nanoparticles and how to overcome it. Nat Nanotechnol 13:65–71. doi:10.1038/s41565-017-0013-y PubMed DOI
Paszek E, Czyz J, Woźnicka O, Jakubiak D, Wojnarowicz J, Łojkowski W, Stepień E. 2012. Zinc oxide nanoparticles impair the integrity of human umbilical vein endothelial cell monolayer in vitro. J Biomed Nanotechnol 8:957–967. doi:10.1166/jbn.2012.1463 PubMed DOI
Daoud NM, Aly MS, Ezzo OH, Ali NA. 2021. Zinc oxide nanoparticles improve testicular steroidogenesis machinery dysfunction in benzo[α]pyrene-challenged rats. Sci Rep 11:11675. doi:10.1038/s41598-021-91226-y PubMed DOI PMC
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120. doi:10.1093/bioinformatics/btu170 PubMed DOI PMC
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. doi:10.1089/cmb.2012.0021 PubMed DOI PMC
Seemann T. 2018. ABRicate: Mass Screening of Contigs for Antimicrobial and Virulence Genes. Department of Microbiology and Immunology. The University of Melbourne, Melbourne, Australia. Available from: https://github com/tseemann/abricate
Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, Møller Aarestrup F, Hasman H. 2014. In silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 58:3895–3903. doi:10.1128/AAC.02412-14 PubMed DOI PMC
Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. 2012. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644. doi:10.1093/jac/dks261 PubMed DOI PMC
Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:1–10. doi:10.1186/gb-2009-10-3-r25 PubMed DOI PMC
Koboldt DC, Chen K, Wylie T, Larson DE, McLellan MD, Mardis ER, Weinstock GM, Wilson RK, Ding L. 2009. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 25:2283–2285. doi:10.1093/bioinformatics/btp373 PubMed DOI PMC
Andrews S. 2010. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Babraham Institute, Cambridge, United Kingdom.
Dyksma S, Pjevac P, Ovanesov K, Mussmann M. 2018. Evidence for H2 consumption by uncultured desulfobacterales in coastal sediments. Environ Microbiol 20:450–461. doi:10.1111/1462-2920.13880 PubMed DOI
Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Nat Prec. doi:10.1038/npre.2010.4282.1 PubMed DOI PMC
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15:550. doi:10.1186/s13059-014-0550-8 PubMed DOI PMC
Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. doi:10.1093/bioinformatics/btp616 PubMed DOI PMC
Team RC. 2022. R: A language and environment for statistical computing
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, Mering C von. 2019. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47:D607–D613. doi:10.1093/nar/gky1131 PubMed DOI PMC
Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, Inuganti A, Griss J, Mayer G, Eisenacher M, Pérez E, Uszkoreit J, Pfeuffer J, Sachsenberg T, Yilmaz S, Tiwary S, Cox J, Audain E, Walzer M, Jarnuczak AF, Ternent T, Brazma A, Vizcaíno JA. 2019. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res 47:D442–D450. doi:10.1093/nar/gky1106 PubMed DOI PMC
Divergent Molecular Responses to Heavy Water in Arabidopsis thaliana Compared to Bacteria and Yeast