{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,25]],"date-time":"2026-08-25T10:41:58Z","timestamp":1787654518860,"version":"build-2736575974"},"reference-count":47,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2022,7,29]],"date-time":"2022-07-29T00:00:00Z","timestamp":1659052800000},"content-version":"vor","delay-in-days":209,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1183848"],"award-info":[{"award-number":["1183848"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000923","name":"Australian Research Council","doi-asserted-by":"publisher","award":["FT170100313"],"award-info":[{"award-number":["FT170100313"]}],"id":[{"id":"10.13039\/501100000923","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,9,21]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Neisseria gonorrhoeae causes the sexually transmitted disease gonorrhoea. The treatment of gonorrhoea is becoming increasingly challenging, as N. gonorrhoeae has developed resistance to antimicrobial agents routinely used in the clinic. Resistance to penicillin is wide-spread partly due to the acquisition of \u03b2-lactamase genes. How N. gonorrhoeae survives an initial exposure to \u03b2-lactams before acquiring resistance genes remains to be understood. Here, using a panel of clinical isolates of N. gonorrhoeae we show that the \u03b2-lactamase enzyme is packaged into outer membrane vesicles (OMVs) by strains expressing blaTEM-1B or blaTEM-106, which protects otherwise susceptible clinical isolates from the \u03b2-lactam drug amoxycillin. We characterized the phenotypes of these clinical isolates of N. gonorrhoeae and the time courses over which the cross-protection of the strains is effective. Imaging and biochemical assays suggest that OMVs promote the transfer of proteins and lipids between bacteria. Thus, N. gonorrhoeae strains secret antibiotic degrading enzymes via OMVs enabling survival of otherwise susceptible bacteria.<\/jats:p>","DOI":"10.1093\/femsml\/uqac013","type":"journal-article","created":{"date-parts":[[2022,7,29]],"date-time":"2022-07-29T12:39:10Z","timestamp":1659098350000},"source":"Crossref","is-referenced-by-count":24,"title":["<i>Neisseria gonorrhoeae<\/i>-derived outer membrane vesicles package \u03b2-lactamases to promote antibiotic resistance"],"prefix":"10.1093","volume":"3","author":[{"given":"Subhash","family":"Dhital","sequence":"first","affiliation":[{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University , Clayton, Australia"},{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pankaj","family":"Deo","sequence":"additional","affiliation":[{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University , Clayton, Australia"},{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manasa","family":"Bharathwaj","sequence":"additional","affiliation":[{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"},{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University , Melbourne, Victoria, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristy","family":"Horan","sequence":"additional","affiliation":[{"name":"Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity , Melbourne, Victoria, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joshua","family":"Nickson","sequence":"additional","affiliation":[{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University , Clayton, Australia"},{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohammad","family":"Azad","sequence":"additional","affiliation":[{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"},{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University , Melbourne, Victoria, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabella","family":"Stuart","sequence":"additional","affiliation":[{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University , Clayton, Australia"},{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seong H","family":"Chow","sequence":"additional","affiliation":[{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University , Clayton, Australia"},{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sachith D","family":"Gunasinghe","sequence":"additional","affiliation":[{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University , Melbourne, Victoria, Australia"},{"name":"European Molecular Biology Laboratory (EMBL) Australia Node in Single Molecule Science, School of Medical Sciences, University of New South Wales , Sydney, New South Wales, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rebecca","family":"Bamert","sequence":"additional","affiliation":[{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"},{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University , Melbourne, Victoria, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian","family":"Li","sequence":"additional","affiliation":[{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"},{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University , Melbourne, Victoria, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0102-7884","authenticated-orcid":false,"given":"Trevor","family":"Lithgow","sequence":"additional","affiliation":[{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"},{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University , Melbourne, Victoria, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benjamin P","family":"Howden","sequence":"additional","affiliation":[{"name":"Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity , Melbourne, Victoria, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2691-0283","authenticated-orcid":false,"given":"Thomas","family":"Naderer","sequence":"additional","affiliation":[{"name":"Infection Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University , Clayton, Australia"},{"name":"Centre to Impact AMR, Monash University , Clayton, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,7,29]]},"reference":[{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1016\/S0140-6736(76)92467-3","article-title":"Penicillinase-producing Neisseria gonorrhoeae","volume":"308","author":"Ashford","year":"1976","journal-title":"Lancet North Am Ed"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"iv28","DOI":"10.1136\/sextrans-2012-050904","article-title":"Monitoring antimicrobial resistance in Neisseria gonorrhoeae in selected countries of the WHO South-East Asia Region between 2009 and 2012: a retrospective analysis","volume":"89","author":"Bala","year":"2013","journal-title":"Sex Transm Infect"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"e0130221","DOI":"10.1128\/mBio.01302-21","article-title":"The Carbapenemase BKC-1 from Klebsiella pneumoniae is adapted for translocation by both the tat and sec translocons","volume":"12","author":"Bharathwaj","year":"2021","journal-title":"mBio"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"806","DOI":"10.3390\/membranes11110806","article-title":"In vivo secretion of beta-lactamase-carrying outer membrane vesicles as a mechanism of beta-lactam therapy failure","volume":"11","author":"Bielaszewska","year":"2021","journal-title":"Membranes"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"7072","DOI":"10.1038\/s41598-017-07288-4","article-title":"Bacterial membrane vesicles transport their DNA cargo into host cells","volume":"7","author":"Bitto","year":"2017","journal-title":"Sci Rep"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1038\/nrmicro3380","article-title":"Molecular mechanisms of antibiotic resistance","volume":"13","author":"Blair","year":"2015","journal-title":"Nat Rev Microbiol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"e1000382","DOI":"10.1371\/journal.ppat.1000382","article-title":"Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles","volume":"5","author":"Bomberger","year":"2009","journal-title":"PLoS Pathog"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"1826","DOI":"10.1093\/infdis\/jiaa003","article-title":"Association of Neisseria gonorrhoeae plasmids with distinct lineages and the economic status of their country of origin","volume":"222","author":"Cehovin","year":"2020","journal-title":"J Infect Dis"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"2201","DOI":"10.1093\/jac\/dkx131","article-title":"Acinetobacter baumannii transfers the blaNDM-1 gene via outer membrane vesicles","volume":"72","author":"Chatterjee","year":"2017","journal-title":"J Antimicrob Chemother"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1093\/jac\/45.1.9","article-title":"Chromosomal beta-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa","volume":"45","author":"Ciofu","year":"2000","journal-title":"J Antimicrob Chemother"},{"key":"2023041117035916400_","first-page":"3238","article-title":"Genetic diversity of blaTEM alleles, antimicrobial susceptibility and molecular epidemiological characteristics of penicillinase-producing Neisseria gonorrhoeae from England and Wales","volume":"70","author":"Cole","year":"2015","journal-title":"J Antimicrob Chemother"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/208239a0","article-title":"Penicillinase synthesis controlled by infectious R factors in enterobacteriaceae","volume":"208","author":"Datta","year":"1965","journal-title":"Nature"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"1418","DOI":"10.1038\/s41564-020-0773-2","article-title":"Mitochondrial dysfunction caused by outer membrane vesicles from Gram-negative bacteria activates intrinsic apoptosis and inflammation","volume":"5","author":"Deo","year":"2020","journal-title":"Nat Microbiol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"e1006945","DOI":"10.1371\/journal.ppat.1006945","article-title":"Outer membrane vesicles from Neisseria gonorrhoeae target PorB to mitochondria and induce apoptosis","volume":"14","author":"Deo","year":"2018","journal-title":"PLoS Pathog"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"1156","DOI":"10.1084\/jem.138.5.1156","article-title":"Release of endotoxin in the form of cell wall blebs during in vitro growth of Neisseria meningitidis","volume":"138","author":"Devoe","year":"1973","journal-title":"J Exp Med"},{"key":"2023041117035916400_","first-page":"298","article-title":"The effect of imipenem and diffusible signaling factors on the secretion of outer membrane vesicles and associated Ax21 proteins in","volume":"6","author":"Devos","year":"2015","journal-title":"Stenotrophomonas maltophilia. 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cargo","volume":"158","author":"Evans","year":"2012","journal-title":"Microbiology"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1038\/nchembio.2083","article-title":"Membrane anchoring stabilizes and favors secretion of New Delhi metallo-beta-lactamase","volume":"12","author":"Gonzalez","year":"2016","journal-title":"Nat Chem Biol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1111\/tra.12488","article-title":"The outer membrane vesicles: secretion system type zero","volume":"18","author":"Guerrero-Mandujano","year":"2017","journal-title":"Traffic"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"2782","DOI":"10.1016\/j.celrep.2018.04.093","article-title":"The WD40 protein BamB mediates coupling of BAM complexes into assembly precincts in the bacterial outer membrane","volume":"23","author":"Gunasinghe","year":"2018","journal-title":"Cell Rep"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"976","DOI":"10.1111\/j.1365-2958.2011.07880.x","article-title":"Targeting of Neisserial PorB to the mitochondrial outer membrane: an insight on the evolution of beta-barrel protein assembly machines","volume":"82","author":"Jiang","year":"2011","journal-title":"Mol Microbiol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"2051","DOI":"10.1099\/13500872-145-8-2051","article-title":"Membrane vesicles derived from Pseudomonas aeruginosa and Shigella flexneri can be integrated into the surfaces of other Gram-negative bacteria","volume":"145","author":"Kadurugamuwa","year":"1999","journal-title":"Microbiology"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"5402","DOI":"10.1038\/s41598-018-23656-0","article-title":"Outer membrane vesicles from \u03b2-lactam-resistant Escherichia coli enable the survival of \u03b2-lactam-susceptible E. coli in the presence of \u03b2-lactam antibiotics","volume":"8","author":"Kim","year":"2018","journal-title":"Sci Rep"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.1021\/pr4009223","article-title":"Molecular characterization and functional analysis of outer membrane vesicles from the antarctic bacterium Pseudomonas syringae suggest a possible response to environmental conditions","volume":"13","author":"Kulkarni","year":"2014","journal-title":"J Proteome Res"},{"key":"2023041117035916400_","first-page":"33934693","article-title":"Australian gonococcal surveillance programme annual report, 2020","volume":"45","author":"Lahra","year":"2021","journal-title":"Commun Dis Intell"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"e0050721","DOI":"10.1128\/AAC.00507-21","article-title":"Specific protein-membrane interactions promote packaging of metallo-beta-lactamases into outer membrane vesicles","volume":"65","author":"Lopez","year":"2021","journal-title":"Antimicrob Agents Chemother"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1186\/1471-2180-11-258","article-title":"Contribution of bacterial outer membrane vesicles to innate bacterial defense","volume":"11","author":"Manning","year":"2011","journal-title":"BMC Microbiol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1016\/j.cmi.2017.04.010","article-title":"Molecular epidemiology of penicillinase-producing Neisseria gonorrhoeae isolates in France","volume":"23","author":"Mica\u00eblo","year":"2017","journal-title":"Clin Microbiol Infect"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"1525","DOI":"10.1111\/cmi.12676","article-title":"Environmentally controlled bacterial vesicle-mediated export","volume":"18","author":"Orench-Rivera","year":"2016","journal-title":"Cell Microbiol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"e00339","DOI":"10.1128\/mBio.00339-12","article-title":"Unexpected diversity of signal peptides in prokaryotes","volume":"3","author":"Payne","year":"2012","journal-title":"mBio"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1016\/S0140-6736(76)92466-1","article-title":"Beta-lactamase-producing, penicillin-resistant gonococcus","volume":"308","author":"Phillips","year":"1976","journal-title":"Lancet North Am Ed"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1128\/AAC.00642-08","article-title":"Sec- and tat-dependent translocation of \u03b2-Lactamases across the Escherichia coli inner membrane","volume":"3","author":"Pradel","year":"2009","journal-title":"Antimicrob Agents Chemother"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"1250","DOI":"10.1128\/JB.01090-13","article-title":"Role for Mycobacterium tuberculosis membrane vesicles in iron acquisition","volume":"196","author":"Prados-Rosales","year":"2014","journal-title":"J Bacteriol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.cub.2013.10.077","article-title":"An ecological network of polysaccharide utilization among human intestinal symbionts","volume":"24","author":"Rakoff-Nahoum","year":"2014","journal-title":"Curr Biol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1146\/annurev-micro-090816-093530","article-title":"Neisseria gonorrhoeae: drug resistance, mouse models, and vaccine development","volume":"71","author":"Rice","year":"2017","journal-title":"Annu Rev Microbiol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"e1006924","DOI":"10.1371\/journal.ppat.1006924","article-title":"Antibiotic interceptors: creating safe spaces for bacteria","volume":"14","author":"Sabnis","year":"2018","journal-title":"PLoS Pathog"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"3845","DOI":"10.1128\/AAC.01772-10","article-title":"Moraxella catarrhalis outer membrane vesicles carry beta-lactamase and promote survival of Streptococcus pneumoniae and Haemophilus influenzae by inactivating amoxicillin","volume":"55","author":"Schaar","year":"2011","journal-title":"Antimicrob Agents Chemother"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1038\/nrmicro3525","article-title":"Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions","volume":"13","author":"Schwechheimer","year":"2015","journal-title":"Nat Rev Microbiol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1093\/jac\/dku466","article-title":"Cephalosporinases associated with outer membrane vesicles released by Bacteroides spp. protect gut pathogens and commensals against beta-lactam antibiotics","volume":"70","author":"Stentz","year":"2015","journal-title":"J Antimicrob Chemother"},{"key":"2023041117035916400_","first-page":"571","article-title":"Interaction of bacterial membrane vesicles with specific species and their potential for delivery to target","volume":"8","author":"Tashiro","year":"2017","journal-title":"Cells Front Microbiol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"670","DOI":"10.3390\/microorganisms8050670","article-title":"The role of bacterial membrane vesicles in the dissemination of antibiotic resistance and as promising carriers for therapeutic agent delivery","volume":"8","author":"Uddin","year":"2020","journal-title":"Microorganisms"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/nrurol.2016.268","article-title":"Antimicrobial-resistant sexually transmitted infections: gonorrhoea and Mycoplasma genitalium","volume":"14","author":"Unemo","year":"2017","journal-title":"Nat Rev Urol"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1128\/CMR.00010-14","article-title":"Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future","volume":"27","author":"Unemo","year":"2014","journal-title":"Clin Microbiol Rev"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1038\/nprot.2007.521","article-title":"Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances","volume":"3","author":"Wiegand","year":"2008","journal-title":"Nat Protoc"},{"key":"2023041117035916400_","doi-asserted-by":"crossref","first-page":"3988","DOI":"10.1038\/s41467-019-12053-4","article-title":"Bridging of Neisseria gonorrhoeae lineages across sexual networks in the HIV pre-exposure prophylaxis 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