Heterogeneity and Genomic Plasticity of Acinetobacter baumannii and Acinetobacter nosocomialis Isolates Recovered from Clinical Samples in India.
Acinetobacter baumannii
/ genetics
Acinetobacter Infections
/ microbiology
India
Humans
Genome, Bacterial
Anti-Bacterial Agents
/ pharmacology
Acinetobacter
/ genetics
Microbial Sensitivity Tests
Virulence Factors
/ genetics
Plasmids
/ genetics
Carbapenems
/ pharmacology
Drug Resistance, Multiple, Bacterial
/ genetics
Genomics
Drug Resistance, Bacterial
/ genetics
Journal
Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448
Informations de publication
Date de publication:
19 Oct 2024
19 Oct 2024
Historique:
received:
22
06
2024
accepted:
07
10
2024
medline:
19
10
2024
pubmed:
19
10
2024
entrez:
19
10
2024
Statut:
epublish
Résumé
Acinetobacter baumannii and Acinetobacter nosocomialis are the imperious pathogens in the intensive care units. We aimed to explore the genomic features of these pathogens to understand the factors influencing their plasticity. Using next-generation sequencing, two carbapenem-resistant A. baumannii (AbaBS-3, AbaETR-4) isolates and a pan-susceptible A. nosocomialis (AbaAS-5) isolate were characterised. All genomes exhibited 94% similarity with a degree of heterogeneity. AbaBS-3 and AbaETR-4 harboured antibiotic resistance gene (ARG) repertoire to most antibiotic classes. Carbapenem resistance was due to blaOXA-23 and blaOXA-66 besides the antibiotic efflux pumps. Diverse mobile genetic elements (MGE), insertion sequences (IS), prophages and virulence determinants with a plethora of stress response genes were identified in all three genomes. Class-1 integron in AbaETR-4, encoded genes that confer resistance to aminoglycosides, phenicol, sulfonamides and disinfectants. Substitutions in LpxACD and PmrCAB of AbaETR-4 confirmed the colistin resistance in vitro. Novel mutations in piuA, responsible for transporting cefiderocol, were found in AbaBS-3 and AbaETR-4. Plasmids carrying toxin-antitoxin systems, ARGs and ISs were present in these genomes. All three genomes harboured diverse protein secretion systems, virulence determinants related to immune evasion, adherence, biofilm formation and iron acquisition systems. AbaAS-5 exclusively harboured serine protease pkf, and CpaA substrate of type-II secretion system but lacked the acinetobactin-iron acquisition system. Our work delivers a holistic genome characterization of A. baumannii, coupled with a trailblazing attempt to study A. nosocomialis from India. The presence of ARGs and potential virulence factors interspersed with MGE is a cause for concern, depicting the dynamic adaptability mediated by genetic recombination.
Identifiants
pubmed: 39425793
doi: 10.1007/s00284-024-03942-z
pii: 10.1007/s00284-024-03942-z
doi:
Substances chimiques
Anti-Bacterial Agents
0
Virulence Factors
0
Carbapenems
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
415Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Imperi F et al (2011) The genomics of Acinetobacter baumannii: insights into genome plasticity, antimicrobial resistance and pathogenicity. IUBMB Life 63(12):1068–1074. https://doi.org/10.1002/iub.531
doi: 10.1002/iub.531
pubmed: 22034231
Nithichanon A et al (2022) Acinetobacter nosocomialis causes as severe disease as Acinetobacter baumannii in Northeast Thailand: underestimated role of A. nosocomialis in infection. Microbiol Spectr 10(6):e0283622. https://doi.org/10.1128/spectrum.02836-22
doi: 10.1128/spectrum.02836-22
pubmed: 36227120
Harding CM, Hennon SW, Feldman MF (2018) Uncovering the mechanisms of Acinetobacter baumannii virulence. Nat Rev Microbiol 16(2):91–102. https://doi.org/10.1038/NRMICRO.2017.148
doi: 10.1038/NRMICRO.2017.148
pubmed: 29249812
Ramisetty BCM, Sudhakari PA (2019) Bacterial ‘grounded’ prophages: hotspots for genetic renovation and innovation. Front Genet. https://doi.org/10.3389/FGENE.2019.00065
doi: 10.3389/FGENE.2019.00065
pubmed: 30809245
pmcid: 6379469
Lee CR et al (2017) Biology of Acinetobacter baumannii: pathogenesis, antibiotic resistance mechanisms, and prospective treatment options. Front Cell Infect Microbiol. https://doi.org/10.3389/FCIMB.2017.00055
doi: 10.3389/FCIMB.2017.00055
pubmed: 29326886
pmcid: 5736563
Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; thirty-second informational supplement, CLSI document M100-S32. CLINICAL AND LABORATORY, 2022. Accessed: Mar. 07, 2024. [Online]. Available: www.clsi.org
Hu Y, He L, Tao X, Meng F, Zhang J (2016) Biofilm may not be necessary for the epidemic spread of Acinetobacter baumannii. Sci Rep 6(1):32066. https://doi.org/10.1038/srep32066
doi: 10.1038/srep32066
pubmed: 27558010
pmcid: 4997352
Gascón E, Merino N, Pagán E, Berdejo D, Pagán R, García-Gonzalo D (2021) Assessment of in vitro biofilms by plate count and crystal violet staining: is one technique enough? Springer, New York, pp 53–63
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069. https://doi.org/10.1093/bioinformatics/btu153
doi: 10.1093/bioinformatics/btu153
pubmed: 24642063
Tatusova T et al (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44(14):6614–6624. https://doi.org/10.1093/nar/gkw569
doi: 10.1093/nar/gkw569
pubmed: 27342282
pmcid: 5001611
Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM (2021) BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol 38(10):4647–4654. https://doi.org/10.1093/molbev/msab199
doi: 10.1093/molbev/msab199
pubmed: 34320186
pmcid: 8476166
Rodriguez-R LM, Konstantinidis KT (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Prepr. https://doi.org/10.7287/peerj.preprints.1900v1
doi: 10.7287/peerj.preprints.1900v1
Jolley KA, Bray JE, Maiden MCJ (2018) Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 3:124. https://doi.org/10.12688/wellcomeopenres.14826.1
doi: 10.12688/wellcomeopenres.14826.1
pubmed: 30345391
pmcid: 6192448
Jolley KA, Maiden MC (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinform 11(1):595. https://doi.org/10.1186/1471-2105-11-595
doi: 10.1186/1471-2105-11-595
Bertels F, Silander OK, Pachkov M, Rainey PB, Van Nimwegen E (2014) Automated reconstruction of whole-genome phylogenies from short-sequence reads. Mol Biol Evol 31(5):1077–1088. https://doi.org/10.1093/MOLBEV/MSU088
doi: 10.1093/MOLBEV/MSU088
pubmed: 24600054
pmcid: 3995342
Olson RD et al (2023) Introducing the bacterial and viral bioinformatics resource center (BV-BRC): a resource combining PATRIC, IRD and ViPR. Nucleic Acids Res 51(D1):D678–D689. https://doi.org/10.1093/nar/gkac1003
doi: 10.1093/nar/gkac1003
pubmed: 36350631
Bortolaia V et al (2020) ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 75(12):3491–3500. https://doi.org/10.1093/jac/dkaa345
doi: 10.1093/jac/dkaa345
pubmed: 32780112
pmcid: 7662176
Alcock BP et al (2023) CARD 2023: expanded curation, support for machine learning, and resistome prediction at the comprehensive antibiotic resistance database. Nucleic Acids Res 51(D1):D690–D699. https://doi.org/10.1093/nar/gkac920
doi: 10.1093/nar/gkac920
pubmed: 36263822
Liu B, Zheng D, Zhou S, Chen L, Yang J (2022) VFDB 2022: a general classification scheme for bacterial virulence factors. Nucleic Acids Res 50(D1):D912–D917. https://doi.org/10.1093/nar/gkab1107
doi: 10.1093/nar/gkab1107
pubmed: 34850947
Madeira F et al (2022) Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res 50(W1):W276–W279. https://doi.org/10.1093/nar/gkac240
doi: 10.1093/nar/gkac240
pubmed: 35412617
pmcid: 9252731
Pejaver V et al (2020) Inferring the molecular and phenotypic impact of amino acid variants with MutPred2. Nat Commun 11(1):5918. https://doi.org/10.1038/s41467-020-19669-x
doi: 10.1038/s41467-020-19669-x
pubmed: 33219223
pmcid: 7680112
van der Graaf-van Bloois L, Wagenaar JA, Zomer AL (2021) RFPlasmid: predicting plasmid sequences from short-read assembly data using machine learning. Microb Genom. https://doi.org/10.1099/mgen.0.000683
doi: 10.1099/mgen.0.000683
pubmed: 34846288
pmcid: 8743549
Schmartz GP et al (2022) PLSDB: advancing a comprehensive database of bacterial plasmids. Nucleic Acids Res 50(D1):D273–D278. https://doi.org/10.1093/nar/gkab1111
doi: 10.1093/nar/gkab1111
pubmed: 34850116
Néron B, Littner E, Haudiquet M, Perrin A, Cury J, Rocha EPC (2022) IntegronFinder 2.0: identification and analysis of integrons across bacteria, with a focus on antibiotic resistance in Klebsiella. Microorganisms. https://doi.org/10.3390/microorganisms10040700
doi: 10.3390/microorganisms10040700
pubmed: 35456751
pmcid: 9024848
Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34:D32-6. https://doi.org/10.1093/nar/gkj014
doi: 10.1093/nar/gkj014
pubmed: 16381877
Arndt D et al (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44(W1):W16-21. https://doi.org/10.1093/nar/gkw387
doi: 10.1093/nar/gkw387
pubmed: 27141966
pmcid: 4987931
Hua X et al (2020) Bautype: capsule and lipopolysaccharide serotype prediction for Acinetobacter baumannii genome. Infect Microbes Dis 2(1):18–25. https://doi.org/10.1097/IM9.0000000000000019
doi: 10.1097/IM9.0000000000000019
King LB, Swiatlo E, Swiatlo A, McDaniel LS (2009) Serum resistance and biofilm formation in clinical isolates of Acinetobacter baumannii. FEMS Immunol Med Microbiol 55(3):414–421. https://doi.org/10.1111/j.1574-695X.2009.00538.x
doi: 10.1111/j.1574-695X.2009.00538.x
pubmed: 19220466
Smoke SM et al (2023) Evolution and transmission of cefiderocol-resistant Acinetobacter baumannii during an outbreak in the burn intensive care unit. Clin Infect Dis 76(3):e1261–e1265. https://doi.org/10.1093/cid/ciac647
doi: 10.1093/cid/ciac647
pubmed: 35974429
King LB, Pangburn MK, McDaniel LS (2013) Serine protease PKF of Acinetobacter baumannii results in serum resistance and suppression of biofilm formation. J Infect Dis 207(7):1128–1134. https://doi.org/10.1093/INFDIS/JIS939
doi: 10.1093/INFDIS/JIS939
pubmed: 23303803
Giardina BJ, Shahzad S, Huang W, Wilks A (2019) Heme uptake and utilization by hypervirulent Acinetobacter baumannii LAC-4 is dependent on a canonical heme oxygenase (abHemO). Arch Biochem Biophys. https://doi.org/10.1016/J.ABB.2019.108066
doi: 10.1016/J.ABB.2019.108066
pubmed: 31398314
pmcid: 6718340
Gheorghe I et al (2021) Subtypes, resistance and virulence platforms in extended-drug resistant Acinetobacter baumannii Romanian isolates. Sci Rep 11(1):1–12. https://doi.org/10.1038/s41598-021-92590-5
doi: 10.1038/s41598-021-92590-5
Traglia G et al (2018) Genome sequence analysis of an extensively drug-resistant Acinetobacter baumannii indigo-pigmented strain depicts evidence of increase genome plasticity. Sci Rep. https://doi.org/10.1038/S41598-018-35377-5
doi: 10.1038/S41598-018-35377-5
pubmed: 30446709
pmcid: 6240043
Kenyon JJ, Holt KE, Pickard D, Dougan G, Hall RM (2014) Insertions in the OCL1 locus of Acinetobacter baumannii lead to shortened lipooligosaccharides. Res Microbiol 165(6):472–475. https://doi.org/10.1016/J.RESMIC.2014.05.034
doi: 10.1016/J.RESMIC.2014.05.034
pubmed: 24861001
pmcid: 4110982
Elhosseiny NM, Attia AS (2018) Acinetobacter: an emerging pathogen with a versatile secretome. Emerg Microbes Infect. https://doi.org/10.1038/S41426-018-0030-4
doi: 10.1038/S41426-018-0030-4
pubmed: 29559620
pmcid: 5861075
Semenec L et al (2023) Cross-protection and cross-feeding between Klebsiella pneumoniae and Acinetobacter baumannii promotes their co-existence. Nat Commun. https://doi.org/10.1038/S41467-023-36252-2
doi: 10.1038/S41467-023-36252-2
pubmed: 36759602
pmcid: 9911699
Vijayakumar S et al (2022) Genomic characterization of mobile genetic elements associated with Carbapenem resistance of Acinetobacter baumannii from India. Front Microbiol 13:869653. https://doi.org/10.3389/FMICB.2022.869653/BIBTEX
doi: 10.3389/FMICB.2022.869653/BIBTEX
pubmed: 35783393
pmcid: 9240704
Roca I, Espinal P, Vila-Fanés X, Vila J (2012) The Acinetobacter baumannii oxymoron: commensal hospital dweller turned pan-drug-resistant menace. Front Microbiol 3:18713. https://doi.org/10.3389/FMICB.2012.00148/BIBTEX
doi: 10.3389/FMICB.2012.00148/BIBTEX
Bharathi SV, Venkataramaiah M, Rajamohan G (2021) Genotypic and phenotypic characterization of novel sequence types of Carbapenem-resistant Acinetobacter baumannii, With heterogeneous resistance determinants and targeted variations in efflux operons. Front Microbiol. https://doi.org/10.3389/fmicb.2021.738371
doi: 10.3389/fmicb.2021.738371
pubmed: 35002996
pmcid: 8735875
Javkar K et al (2021) Whole-genome assessment of clinical Acinetobacter baumannii isolates uncovers potentially novel factors influencing carbapenem resistance. Front Microbiol 12:714284. https://doi.org/10.3389/fmicb.2021.714284
doi: 10.3389/fmicb.2021.714284
pubmed: 34659144
pmcid: 8518998
Marano V et al (2020) Identification of pmrB mutations as putative mechanism for colistin resistance in A. baumannii strains isolated after in vivo colistin exposure. Microb Pathog 142:104058. https://doi.org/10.1016/j.micpath.2020.104058
doi: 10.1016/j.micpath.2020.104058
pubmed: 32058026
Malik S, Kaminski M, Landman D, Quale J (2020) Cefiderocol resistance in Acinetobacter baumannii: roles of β-lactamases, siderophore receptors, and penicillin binding protein 3. Antimicrob Agents Chemother 64(11):e01221-e1320. https://doi.org/10.1128/AAC.01221-20
doi: 10.1128/AAC.01221-20
pubmed: 32868330
pmcid: 7577126
Brovedan MA, Cameranesi MM, Limansky AS, Morán-Barrio J, Marchiaro P, Repizo GD (2020) What do we know about plasmids carried by members of the Acinetobacter genus? World J Microbiol Biotechnol 36(8):109. https://doi.org/10.1007/s11274-020-02890-7
doi: 10.1007/s11274-020-02890-7
pubmed: 32656745
Hipólito A, García-Pastor L, Vergara E, Jové T, Escudero JA (2023) Profile and resistance levels of 136 integron resistance genes. NPJ Antimicrob Resist 1(1):13. https://doi.org/10.1038/s44259-023-00014-3
doi: 10.1038/s44259-023-00014-3
Costa AR, Monteiro R, Azeredo J (2018) Genomic analysis of Acinetobacter baumannii prophages reveals remarkable diversity and suggests profound impact on bacterial virulence and fitness. Sci Rep 8(1):1–11. https://doi.org/10.1038/s41598-018-33800-5
doi: 10.1038/s41598-018-33800-5
Nho JS et al (2015) Acinetobacter nosocomialis secretes outer membrane vesicles that induce epithelial cell death and host inflammatory responses. Microb Pathog 81:39–45. https://doi.org/10.1016/J.MICPATH.2015.03.012
doi: 10.1016/J.MICPATH.2015.03.012
pubmed: 25778390
Fiester SE, Actis LA (2013) Stress responses in the opportunistic pathogen Acinetobacter baumannii. Future Microbiol 8(3):353–365. https://doi.org/10.2217/FMB.12.150
doi: 10.2217/FMB.12.150
pubmed: 23464372
Biselli E, Schink SJ, Gerland U (2020) Slower growth of Escherichia coli leads to longer survival in carbon starvation due to a decrease in the maintenance rate. Mol Syst Biol 16(6):9478. https://doi.org/10.15252/MSB.20209478/SUPPL_FILE/MSB209478-SUP-0005-TABLEEV4.DOCX
doi: 10.15252/MSB.20209478/SUPPL_FILE/MSB209478-SUP-0005-TABLEEV4.DOCX
Roux D et al (2015) Fitness cost of antibiotic susceptibility during bacterial infection. Sci Transl Med. https://doi.org/10.1126/SCITRANSLMED.AAB1621/SUPPL_FILE/7-297RA114_SM.PDF
doi: 10.1126/SCITRANSLMED.AAB1621/SUPPL_FILE/7-297RA114_SM.PDF
pubmed: 26203082