{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,4]],"date-time":"2026-03-04T04:33:14Z","timestamp":1772598794576,"version":"3.50.1"},"reference-count":72,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2023,4,18]],"date-time":"2023-04-18T00:00:00Z","timestamp":1681776000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Manchester Metropolitan University"},{"name":"The University of Manchester Health Research Accelerator"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>With the increase in antimicrobial resistance, there is an urgent need to find new antimicrobials. Four particulate antimicrobial compounds, graphite (G), graphene oxide (GO), silver\u2013graphene oxide (Ag-GO) and zinc oxide\u2013graphene oxide (ZnO-GO) were tested against Enterococcus faecium, Escherichia coli, Klebsiella pneumoniae and Staphylococcus aureus. The antimicrobial effects on the cellular ultrastructure were determined using Fourier transform infrared spectroscopy (FTIR), and selected FTIR spectral metrics correlated with cell damage and death arising from exposure to the GO hybrids. Ag-GO caused the most severe damage to the cellular ultrastructure, whilst GO caused intermediate damage. Graphite exposure caused unexpectedly high levels of damage to E. coli, whereas ZnO-GO exposure led to relatively low levels of damage. The Gram-negative bacteria demonstrated a stronger correlation between FTIR metrics, indicated by the perturbation index and the minimal bactericidal concentration (MBC). The blue shift of the combined ester carbonyl and amide I band was stronger for the Gram-negative varieties. FTIR metrics tended to provide a better assessment of cell damage based on correlation with cellular imaging and indicated that damage to the lipopolysaccharide, peptidoglycan and phospholipid bilayers had occurred. Further investigations into the cell damage caused by the GO-based materials will allow the development of this type of carbon-based multimode antimicrobials.<\/jats:p>","DOI":"10.3390\/antibiotics12040776","type":"journal-article","created":{"date-parts":[[2023,4,19]],"date-time":"2023-04-19T01:39:05Z","timestamp":1681868345000},"page":"776","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Analysis of Cellular Damage Resulting from Exposure of Bacteria to Graphene Oxide and Hybrids Using Fourier Transform Infrared Spectroscopy"],"prefix":"10.3390","volume":"12","author":[{"given":"Christopher M.","family":"Liauw","sequence":"first","affiliation":[{"name":"Microbiology at Interfaces Group, School of Healthcare Sciences, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Misha","family":"Vaidya","sequence":"additional","affiliation":[{"name":"Microbiology at Interfaces Group, School of Healthcare Sciences, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7062-6901","authenticated-orcid":false,"given":"Anthony J.","family":"Slate","sequence":"additional","affiliation":[{"name":"Department of Life Sciences, University of Bath, Claverton Down, Bath BA2 7AY, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Niall A.","family":"Hickey","sequence":"additional","affiliation":[{"name":"Microbiology at Interfaces Group, School of Healthcare Sciences, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Steven","family":"Ryder","sequence":"additional","affiliation":[{"name":"Microbiology at Interfaces Group, School of Healthcare Sciences, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3122-3381","authenticated-orcid":false,"given":"Emiliano","family":"Mart\u00ednez-Peri\u00f1\u00e1n","sequence":"additional","affiliation":[{"name":"Departamento de Qu\u00edmica Anal\u00edtica y An\u00e1lisis Instrumental, Universidad Aut\u00f3noma de Madrid, 28049 Madrid, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5255-5425","authenticated-orcid":false,"given":"Andrew J.","family":"McBain","sequence":"additional","affiliation":[{"name":"School of Health Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester M13 9PT, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0756-9764","authenticated-orcid":false,"given":"Craig E.","family":"Banks","sequence":"additional","affiliation":[{"name":"Faculty of Science and Engineering, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6001-6686","authenticated-orcid":false,"given":"Kathryn A.","family":"Whitehead","sequence":"additional","affiliation":[{"name":"Microbiology at Interfaces Group, School of Healthcare Sciences, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1177\/2042098614554919","article-title":"Antimicrobial resistance: Risk associated with antibiotic overuse and initiatives to reduce the problem","volume":"5","author":"Llor","year":"2014","journal-title":"Ther. Adv. Drug Saf."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"S82","DOI":"10.1086\/499406","article-title":"The Relationship between Antimicrobial Resistance and Patient Outcomes: Mortality, Length of Hospital Stay, and Health Care Costs","volume":"42","author":"Cosgrove","year":"2006","journal-title":"Clin. Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1093\/jac\/49.1.11","article-title":"Biocide abuse and antimicrobial resistance\u2014A cause for concern?","volume":"49","author":"Fraise","year":"2002","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Pal, C., Bengtsson-Palme, J., Kristiansson, E., and Larsson, D.G.J. (2015). Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genom., 16.","DOI":"10.1186\/s12864-015-2153-5"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2241","DOI":"10.1093\/jac\/dkv109","article-title":"Parallel evolutionary pathways to antibiotic resistance selected by biocide exposure","volume":"70","author":"Webber","year":"2015","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Eriksson, J., Gilek, M., and Rud\u00e9n, C. (2010). Regulating Chemical Risks: European and Global Challenges, Springer Science & Business Media.","DOI":"10.1007\/978-90-481-9428-5"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1038\/nrmicro3028","article-title":"Antimicrobial activity of metals: Mechanisms, molecular targets and applications","volume":"11","author":"Lemire","year":"2013","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_8","first-page":"272","article-title":"Copper, an ancient remedy returning to fight microbial, fungal and viral infections","volume":"3","author":"Borkow","year":"2009","journal-title":"Curr. Chem. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1007\/BF03215464","article-title":"Medical uses of gold compounds: Past, present and future","volume":"29","author":"Pricker","year":"1996","journal-title":"Gold Bull."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1089\/sur.2008.9941","article-title":"History of the Medical Use of Silver","volume":"10","author":"Alexander","year":"2009","journal-title":"Surg. Infect."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.jhin.2015.09.008","article-title":"Antimicrobial surfaces to prevent healthcare-associated infections: A systematic review","volume":"92","author":"Muller","year":"2016","journal-title":"J. Hosp. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.biotechadv.2008.09.002","article-title":"Silver nanoparticles as a new generation of antimicrobials","volume":"27","author":"Rai","year":"2009","journal-title":"Biotechnol. Adv."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3819","DOI":"10.1039\/b818698g","article-title":"Antimicrobial surfaces and their potential in reducing the role of the inanimate environment in the incidence of hospital-acquired infections","volume":"19","author":"Page","year":"2009","journal-title":"J. Mater. Chem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1595\/147106712X651748","article-title":"Final Analysis: Palladium in Temporary and Permanently Implantable Medical Devices","volume":"56","author":"Woodward","year":"2012","journal-title":"Platin. Met. Rev."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Baltzer, N., and Copponnex, T. (2014). Precious Metals for Biomedical Applications, Elsevier Science & Technology.","DOI":"10.1533\/9780857099051.1.3"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1595\/147106711X566816","article-title":"A Healthy Future: Platinum in Medical Applications","volume":"55","author":"Cowley","year":"2011","journal-title":"Platin. Met. Rev."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1462","DOI":"10.1016\/j.jdent.2015.10.010","article-title":"Anti-biofilm activity of zinc oxide and hydroxyapatite nanoparticles as dental implant coating materials","volume":"43","author":"Abdulkareem","year":"2015","journal-title":"J. Dent."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1007\/s40820-015-0040-x","article-title":"Review on Zinc Oxide Nanoparticles: Antibacterial Activity and Toxicity Mechanism","volume":"7","author":"Sirelkhatim","year":"2015","journal-title":"Nano-Micro Lett."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.nano.2007.02.001","article-title":"Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli","volume":"3","author":"Shahverdi","year":"2007","journal-title":"Nanomed. Nanotechnol. Biol. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4873","DOI":"10.1021\/ja5011338","article-title":"Antimicrobial Metallopolymers and Their Bioconjugates with Conventional Antibiotics against Multidrug-Resistant Bacteria","volume":"136","author":"Zhang","year":"2014","journal-title":"J. Am. Chem. Soc."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"5911","DOI":"10.1038\/s41598-017-05976-9","article-title":"Antimicrobial Efficacy and Synergy of Metal Ions against Enterococcus faecium, Klebsiella pneumoniae and Acinetobacter baumannii in Planktonic and Biofilm Phenotypes","volume":"7","author":"Vaidya","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"5731","DOI":"10.1021\/nn101390x","article-title":"Toxicity of graphene and graphene oxide nanowalls against bacteria","volume":"4","author":"Akhavan","year":"2010","journal-title":"ACS Nano"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"317","DOI":"10.2217\/nnm.10.158","article-title":"Graphene in biomedicine: Opportunities and challenges","volume":"6","author":"Feng","year":"2011","journal-title":"Nanomedicine"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"6971","DOI":"10.1021\/nn202451x","article-title":"Antibacterial Activity of Graphite, Graphite Oxide, Graphene Oxide, and Reduced Graphene Oxide: Membrane and Oxidative Stress","volume":"5","author":"Liu","year":"2011","journal-title":"ACS Nano"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Banks, C., and Brownson, D. (2017). Advanced 2D Material\u2013Characterisation, Production and Applications, CRC Press.","DOI":"10.1201\/9781315152042"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3163","DOI":"10.1016\/j.biomaterials.2003.10.010","article-title":"The effects of amorphous carbon films deposited on polyethylene terephthalate on bacterial adhesion","volume":"25","author":"Wang","year":"2004","journal-title":"Biomaterials"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1016\/S1286-4579(02)01604-0","article-title":"Structure and function of lipopolysaccharides","volume":"4","author":"Erridge","year":"2002","journal-title":"Microbes Infect."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/j.bbamem.2014.05.031","article-title":"Peptidoglycan architecture of Gram-positive bacteria by solid-state NMR","volume":"1848","author":"Kim","year":"2015","journal-title":"Biochim. Biophys. Acta (BBA)-Biomembr."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1146\/annurev.mi.37.100183.002441","article-title":"Structure, function, and assembly of cell walls of gram-positive bacteria","volume":"37","author":"Shockman","year":"1983","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_30","unstructured":"Singleton, P. (2004). Bacteria in Biology, Biotechnology and Medicine, John Wiley & Sons."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"906","DOI":"10.7326\/0003-4819-111-11-906","article-title":"Urinary tract infections in women: Diagnosis and treatment","volume":"111","author":"Johnson","year":"1989","journal-title":"Ann. Intern. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1016\/S1047-2797(00)00072-7","article-title":"Urinary Tract Infection: Self-Reported Incidence and Associated Costs","volume":"10","author":"Foxman","year":"2000","journal-title":"Ann. Epidemiol."},{"key":"ref_33","unstructured":"Ryan, K.J., and Ray, C.G. (2004). Medical Microbiology, McGraw Hill."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1086\/432803","article-title":"Overview of Nosocomial Infections Caused by Gram-Negative Bacilli","volume":"41","author":"Weinstein","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1038\/nrmicro3432","article-title":"Urinary tract infections: Epidemiology, mechanisms of infection and treatment options","volume":"13","author":"Walker","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1111\/j.1574-695X.2008.00383.x","article-title":"Emergence of CC17 Enterococcus faecium: From commensal to hospital-adapted pathogen","volume":"52","author":"Top","year":"2008","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1038\/nrmicro2761","article-title":"The rise of the Enterococcus: Beyond vancomycin resistance","volume":"10","author":"Arias","year":"2012","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1586\/14787210.6.5.637","article-title":"Emergence and management of drug-resistant enterococcal infections","volume":"6","author":"Arias","year":"2008","journal-title":"Expert Rev. Anti-Infect. Ther."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1126\/science.1171700","article-title":"Topographical and Temporal Diversity of the Human Skin Microbiome","volume":"324","author":"Grice","year":"2009","journal-title":"Science"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3705","DOI":"10.1002\/1873-3468.12455","article-title":"Composition and immunological significance of the upper respiratory tract microbiota","volume":"590","author":"Schenck","year":"2016","journal-title":"FEBS Lett."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1128\/CMR.00134-14","article-title":"Staphylococcus aureus Infections: Epidemiology, Pathophysiology, Clinical Manifestations, and Management","volume":"28","author":"Tong","year":"2015","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1115","DOI":"10.1007\/s00253-009-2159-5","article-title":"Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli","volume":"85","author":"Li","year":"2009","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.jcis.2004.02.012","article-title":"Silver nanoparticles as antimicrobial agent: A case study on E. coli as a model for Gram-negative bacteria","volume":"275","author":"Sondi","year":"2004","journal-title":"J. Colloid Interface Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2171","DOI":"10.1128\/AEM.02001-07","article-title":"Antibacterial Activity and Mechanism of Action of the Silver Ion in Staphylococcus aureus and Escherichia coli","volume":"74","author":"Jung","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.nano.2006.12.001","article-title":"Antimicrobial effects of silver nanoparticles","volume":"3","author":"Kim","year":"2007","journal-title":"Nanomed. Nanotechnol. Boil. Med."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1139\/m74-135","article-title":"The effect of silver ions on the respiratory chain of Escherichia coli","volume":"20","author":"Bragg","year":"1974","journal-title":"Can. J. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2767","DOI":"10.2147\/IJN.S24805","article-title":"Antimicrobial applications of nanotechnology: Methods and literature","volume":"7","author":"Webster","year":"2012","journal-title":"Int. J. Nanomed."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2325","DOI":"10.1128\/AEM.02149-10","article-title":"Antibacterial Activity and Mechanism of Action of Zinc Oxide Nanoparticles against Campylobacter jejuni","volume":"77","author":"Xie","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/s10856-008-3548-5","article-title":"Role of size scale of ZnO nanoparticles and microparticles on toxicity toward bacteria and osteoblast cancer cells","volume":"20","author":"Nair","year":"2008","journal-title":"J. Mater. Sci. Mater. Med."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"035004","DOI":"10.1088\/1468-6996\/9\/3\/035004","article-title":"Enhanced bioactivity of ZnO nanoparticles\u2014An antimicrobial study","volume":"9","author":"Padmavathy","year":"2008","journal-title":"Sci. Technol. Adv. Mater."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1879","DOI":"10.1039\/C3NR04941H","article-title":"Graphene oxide exhibits broad-spectrum antimicrobial activity against bacterial phytopathogens and fungal conidia by intertwining and membrane perturbation","volume":"6","author":"Chen","year":"2013","journal-title":"Nanoscale"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"7226","DOI":"10.1021\/acsnano.5b02067","article-title":"Antimicrobial Properties of Graphene Oxide Nanosheets: Why Size Matters","volume":"9","author":"Perreault","year":"2015","journal-title":"ACS Nano"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1038\/nnano.2013.125","article-title":"Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets","volume":"8","author":"Tu","year":"2013","journal-title":"Nat. Nanotechnol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"17280","DOI":"10.1021\/jp3047054","article-title":"Antibacterial Efficiency of Graphene Nanosheets against Pathogenic Bacteria via Lipid Peroxidation","volume":"116","author":"Krishnamoorthy","year":"2012","journal-title":"J. Phys. Chem. C"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1096\/fasebj.8.2.8119492","article-title":"Bacterial endotoxin: Molecular relationships of structure to activity and function","volume":"8","author":"Rietschel","year":"1994","journal-title":"FASEB J."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"a000414","DOI":"10.1101\/cshperspect.a000414","article-title":"The bacterial cell envelope","volume":"2","author":"Silhavy","year":"2010","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"4404","DOI":"10.1073\/pnas.0510182103","article-title":"Three-dimensional structure of the bacterial cell wall peptidoglycan","volume":"103","author":"Meroueh","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1111\/j.1574-6976.2007.00094.x","article-title":"Peptidoglycan structure and architecture","volume":"32","author":"Vollmer","year":"2008","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1126\/science.7824948","article-title":"Structural Basis for Sugar Translocation Through Maltoporin Channels at 3.1 \u00c5 Resolution","volume":"267","author":"Schirmer","year":"1995","journal-title":"Science"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1146\/annurev.micro.57.030502.090832","article-title":"How Bacteria Assemble Flagella","volume":"57","author":"Macnab","year":"2003","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"7173","DOI":"10.1073\/pnas.0900693106","article-title":"The assembled structure of a complete tripartite bacterial multidrug efflux pump","volume":"106","author":"Symmons","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1128\/MMBR.63.1.174-229.1999","article-title":"Surface Proteins of Gram-Positive Bacteria and Mechanisms of Their Targeting to the Cell Wall Envelope","volume":"63","author":"Navarre","year":"1999","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"11586","DOI":"10.1074\/jbc.M600114200","article-title":"Aslfm, the D-Aspartate Ligase Responsible for the Addition of D-Aspartic Acid onto the Peptidoglycan Precursor of Enterococcus faecium","volume":"281","author":"Bellais","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"9859","DOI":"10.1021\/bi970495d","article-title":"Structure and Dynamics of Pentaglycyl Bridges in the Cell Walls of Staphylococcus aureus by 13C\u2212 15N REDOR NMR","volume":"36","author":"Tong","year":"1997","journal-title":"Biochemistry"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"35243","DOI":"10.1038\/srep35243","article-title":"Toxicity of ZnO and TiO2 to Escherichia coli cells","volume":"6","author":"Leung","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1111\/jam.12423","article-title":"Interaction of Al2O3 nanoparticles with Escherichia coli and their cell envelope biomolecules","volume":"116","author":"Ansari","year":"2014","journal-title":"J. Appl. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.ibiod.2017.06.020","article-title":"Antimicrobial activity of graphene oxide-metal hybrids","volume":"123","author":"Whitehead","year":"2017","journal-title":"Int. Biodeterior. Biodegrad."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1339","DOI":"10.1021\/ja01539a017","article-title":"Preparation of graphitic oxide","volume":"80","author":"Hummers","year":"1958","journal-title":"J. Am. Chem. Soc."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"4298","DOI":"10.1007\/s10854-015-2982-7","article-title":"Microstructural, crystallographic and optical characterizations of Cu-doped ZnO nanoparticles co-doped with Ni","volume":"26","author":"Anandan","year":"2015","journal-title":"J. Mater. Sci. Mater. Electron."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.scriptamat.2011.10.016","article-title":"Varistor effect in Ag\u2013graphene\/epoxy resin nanocomposites","volume":"66","author":"Liu","year":"2012","journal-title":"Scr. Mater."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1016\/j.colsurfb.2017.10.008","article-title":"Production of hybrid macro\/micro\/nano surface structures on Ti6Al4V surfaces by picosecond laser surface texturing and their antifouling characteristics","volume":"160","author":"Rajab","year":"2017","journal-title":"Colloids Surf. B Biointerfaces"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1017\/S002217240001158X","article-title":"The estimation of the bactericidal power of the blood","volume":"38","author":"Miles","year":"1938","journal-title":"Epidemiol. Infect."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/4\/776\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:18:31Z","timestamp":1760123911000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/4\/776"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,18]]},"references-count":72,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["antibiotics12040776"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics12040776","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,18]]}}}