Development of a novel core genome MLST scheme for tracing multidrug resistant Staphylococcus capitis.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
22 07 2022
Historique:
received: 03 12 2021
accepted: 08 07 2022
entrez: 22 7 2022
pubmed: 23 7 2022
medline: 27 7 2022
Statut: epublish

Résumé

Staphylococcus capitis, which causes bloodstream infections in neonatal intensive care units, is a common cause of healthcare-associated infections. Thus, a standardized high-resolution typing method to document the transmission and dissemination of multidrug-resistant S. capitis isolates is required. We aimed to establish a core genome multilocus sequence typing (cgMLST) scheme to surveil S. capitis. The cgMLST scheme was defined based on primary and validation genome sets and tested with outbreaks of linezolid-resistant isolates and a validation set. Phylogenetic analysis was performed to investigate the population structure and compare it with the result of cgMLST analysis. The S. capitis population consists of 1 dominant, NRCS-A, and 4 less common clones. In this work, a multidrug-resistant clone (L clone) with linezolid resistance is identified. With the features of type III SCCmec and multiple copies of mutations of G2576T and C2104T in the 23S rRNA, the L clone has been spreading silently across China.

Identifiants

pubmed: 35869070
doi: 10.1038/s41467-022-31908-x
pii: 10.1038/s41467-022-31908-x
pmc: PMC9307846
doi:

Substances chimiques

Anti-Bacterial Agents 0
Linezolid ISQ9I6J12J

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4254

Informations de copyright

© 2022. The Author(s).

Références

Cui, B., Smooker, P. M., Rouch, D. A., Daley, A. J. & Deighton, M. A. Differences between two clinical Staphylococcus capitis subspecies as revealed by biofilm, antibiotic resistance, and pulsed-field gel electrophoresis profiling. J. Clin. Microbiol. 51, 9–14 (2013).
pubmed: 23052315 pmcid: 3536240 doi: 10.1128/JCM.05124-11
Tevell, S., Hellmark, B., Nilsdotter-Augustinsson, Å. & Söderquist, B. Staphylococcus capitis isolated from prosthetic joint infections. Eur. J. Clin. Microbiol. Infect. Dis. 36, 115–122 (2017).
pubmed: 27680718 doi: 10.1007/s10096-016-2777-7
Van Der Zwet, W. C. et al. Nosocomial spread of a Staphylococcus capitis strain with heteroresistance to vancomycin in a neonatal intensive care unit. J. Clin. Microbiol. 40, 2520–2525 (2002).
doi: 10.1128/JCM.40.7.2520-2525.2002
Rasigade, J.-P. et al. Methicillin-resistant Staphylococcus capitis with reduced vancomycin susceptibility causes late-onset sepsis in intensive care neonates. PLoS One 7, e31548 (2012).
pubmed: 22348102 pmcid: 3279402 doi: 10.1371/journal.pone.0031548
Brodie, S. B. et al. Occurrence of nosocomial bloodstream infections in six neonatal intensive care units. Pediatr. Infect. Dis. J. 19, 56–65 (2000).
pubmed: 10643852 doi: 10.1097/00006454-200001000-00012
Stoll, B. J. et al. Late-onset sepsis in very low birth weight neonates: The experience of the NICHD Neonatal Research Network. Pediatrics 110, 285–291 (2002).
pubmed: 12165580 doi: 10.1542/peds.110.2.285
Wirth, T. et al. Niche specialization and spread of Staphylococcus capitis involved in neonatal sepsis. Nat. Microbiol. 5, 735–745 (2020).
pubmed: 32341568 doi: 10.1038/s41564-020-0676-2
Laurent, F. & Butin, M. Staphylococcus capitis and NRCS-A clone: The story of an unrecognized pathogen in neonatal intensive care units. Clin. Microbiol. Infect. 25, 1081–1085 (2019).
pubmed: 30928561 doi: 10.1016/j.cmi.2019.03.009
Tevell, S. et al. Presence of the neonatal Staphylococcus capitis outbreak clone (NRCS-A) in prosthetic joint infections. Sci. Rep. 10, 1–8 (2020).
doi: 10.1038/s41598-020-79225-x
Leopold, S. R., Goering, R. V., Witten, A., Harmsen, D. & Mellmann, A. Bacterial whole-genome sequencing revisited: Portable, scalable, and standardized analysis for typing and detection of virulence and antibiotic resistance genes. J. Clin. Microbiol. 52, 2365–2370 (2014).
pubmed: 24759713 pmcid: 4097726 doi: 10.1128/JCM.00262-14
Jamet, A. et al. High-resolution typing of Staphylococcus epidermidis based on core genome multilocus sequence typing to investigate the hospital spread of multidrug-resistant clones. J. Clin. Microbiol. 59, e02454–02420 (2021).
pubmed: 33328176 pmcid: 8106705 doi: 10.1128/JCM.02454-20
Liu, S. et al. A core genome multilocus sequence typing scheme for Streptococcus mutans. Msphere 5, e00348–00320 (2020).
pubmed: 32641425 pmcid: 7343978 doi: 10.1128/mSphere.00348-20
Zhou, H., Liu, W., Qin, T., Liu, C. & Ren, H. Defining and evaluating a core genome multilocus sequence typing scheme for whole-genome sequence-based typing of Klebsiella pneumoniae. Front. Microbiol. 8, 371 (2017).
pubmed: 28337187 pmcid: 5340756
Moura, A. et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat. Microbiol. 2, 1–10 (2016).
Ruppitsch, W. et al. Defining and evaluating a core genome multilocus sequence typing scheme for whole-genome sequence-based typing of Listeria monocytogenes. J. Clin. Microbiol. 53, 2869–2876 (2015).
pubmed: 26135865 pmcid: 4540939 doi: 10.1128/JCM.01193-15
Stenmark, B., Hellmark, B. & Söderquist, B. Genomic analysis of Staphylococcus capitis isolated from blood cultures in neonates at a neonatal intensive care unit in Sweden. Eur. J. Clin. Microbiol. Infect. Dis. 38, 2069–2075 (2019).
pubmed: 31396832 pmcid: 6800862 doi: 10.1007/s10096-019-03647-3
Ding, L., Li, P., Yang, Y., Lin, D. & Xu, X. The epidemiology and molecular characteristics of linezolid-resistant Staphylococcus capitis in Huashan Hospital, Shanghai. J. Med. Microbiol. 69, 1079–1088 (2020).
pubmed: 32729813 doi: 10.1099/jmm.0.001234
Li, X. et al. Whole genome sequence and comparative genomic analysis of multidrug-resistant Staphylococcus capitis subsp. urealyticus strain LNZR-1. Gut Pathog. 6, 1–8 (2014).
doi: 10.1186/s13099-014-0045-x
Butin, M. et al. Emergence and dissemination of a linezolid-resistant Staphylococcus capitis clone in Europe. J. Antimicrobial Chemother. 72, 1014–1020 (2017).
Gu, B., Kelesidis, T., Tsiodras, S., Hindler, J. & Humphries, R. M. The emerging problem of linezolid-resistant Staphylococcus. J. Antimicrobial Chemother. 68, 4–11 (2013).
doi: 10.1093/jac/dks354
Meka, V. G. et al. Linezolid resistance in sequential Staphylococcus aureus isolates associated with a T2500A mutation in the 23S rRNA gene and loss of a single copy of rRNA. J. Infect. Dis. 190, 311–317 (2004).
pubmed: 15216466 doi: 10.1086/421471
Long, K. S., Poehlsgaard, J., Kehrenberg, C., Schwarz, S. & Vester, B. The Cfr rRNA methyltransferase confers resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A antibiotics. Antimicrobial Agents Chemother. 50, 2500–2505 (2006).
doi: 10.1128/AAC.00131-06
Tonkin-Hill, G. et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol. 21, 1–21 (2020).
doi: 10.1186/s13059-020-02090-4
Liu, Y. et al. Molecular evidence for spread of two major methicillin-resistant Staphylococcus aureus clones with a unique geographic distribution in Chinese hospitals. Antimicrobial Agents Chemother. 53, 512–518 (2009).
doi: 10.1128/AAC.00804-08
Sun, L. et al. Characterization of vanM carrying clinical Enterococcus isolates and diversity of the suppressed vanM gene cluster. Infect., Genet. Evolution 68, 145–152 (2019).
doi: 10.1016/j.meegid.2018.12.015
Li, W. et al. Large outbreak of herpangina in children caused by enterovirus in summer of 2015 in Hangzhou, China. Sci. Rep. 6, 1–5 (2016).
Schwarz, S. et al. Lincosamides, streptogramins, phenicols, and pleuromutilins: Mode of action and mechanisms of resistance. Cold Spring Harb. Perspect. Med. 6, a027037 (2016).
pubmed: 27549310 pmcid: 5088508 doi: 10.1101/cshperspect.a027037
Cai, J. C., Hu, Y. Y., Zhou, H. W., Chen, G.-X. & Zhang, R. Dissemination of the same cfr-carrying plasmid among methicillin-resistant Staphylococcus aureus and coagulase-negative staphylococcal isolates in China. Antimicrobial Agents Chemother. 59, 3669–3671 (2015).
doi: 10.1128/AAC.04580-14
Matyi, S. et al. Isolation and characterization of Staphylococcus aureus strains from a Paso del Norte dairy. J. Dairy Sci. 96, 3535–3542 (2013).
pubmed: 23608491 pmcid: 5226338 doi: 10.3168/jds.2013-6590
Wu, D. et al. Characterization of an ST5-SCCmec II-t311 methicillin-resistant Staphylococcus aureus strain with a widespread cfr-positive plasmid. J. Infect. Chemother. 26, 699–705 (2020).
pubmed: 32245640 doi: 10.1016/j.jiac.2020.02.018
Yang, X.-J. et al. Emergence of cfr-harbouring coagulase-negative staphylococci among patients receiving linezolid therapy in two hospitals in China. J. Med. Microbiol. 62, 845–850 (2013).
pubmed: 23449871 doi: 10.1099/jmm.0.051003-0
Friedman, N. D., Temkin, E. & Carmeli, Y. The negative impact of antibiotic resistance. Clin. Microbiol. Infect. 22, 416–422 (2016).
pubmed: 26706614 doi: 10.1016/j.cmi.2015.12.002
San Millan, A. & Maclean, R. C. Fitness costs of plasmids: A limit to plasmid transmission. Microbiol. Spectrum 5, 5.5. 02 (2017).
Shariati, A. et al. The global prevalence of Daptomycin, Tigecycline, Quinupristin/Dalfopristin, and Linezolid-resistant Staphylococcus aureus and coagulase–negative staphylococci strains: A systematic review and meta-analysis. Antimicrobial Resistance Infect. Control 9, 1–20 (2020).
doi: 10.1186/s13756-020-00714-9
Pritchard, L., Glover, R. H., Humphris, S., Elphinstone, J. G. & Toth, I. K. Genomics and taxonomy in diagnostics for food security: Soft-rotting enterobacterial plant pathogens. Anal. Methods 8, 12–24 (2016).
doi: 10.1039/C5AY02550H
Seemann, T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).
pubmed: 24642063 doi: 10.1093/bioinformatics/btu153
Johnson, M. et al. NCBI BLAST: A better web interface. Nucleic Acids Res. 36, W5–W9 (2008).
pubmed: 18440982 pmcid: 2447716 doi: 10.1093/nar/gkn201
Jünemann, S. et al. Updating benchtop sequencing performance comparison. Nat. Biotechnol. 31, 294–296 (2013).
pubmed: 23563421 doi: 10.1038/nbt.2522
Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
pubmed: 9254694 pmcid: 146917 doi: 10.1093/nar/25.17.3389
Neumann, B. et al. A core genome multilocus sequence typing scheme for Enterococcus faecalis. J. Clin. Microbiol. 57, e01686–01618 (2019).
pubmed: 30651394 pmcid: 6425188 doi: 10.1128/JCM.01686-18
Earls, M. R. et al. Intra-hospital, inter-hospital, and intercontinental spread of ST78 MRSA from two neonatal intensive care unit outbreaks established using whole-genome sequencing. Front. Microbiol. 9, 1485 (2018).
pubmed: 30022976 pmcid: 6039561 doi: 10.3389/fmicb.2018.01485
Minh, B. Q. et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).
pubmed: 32011700 pmcid: 7182206 doi: 10.1093/molbev/msaa015
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res. 47, W256–W259 (2019).
pubmed: 30931475 pmcid: 6602468 doi: 10.1093/nar/gkz239
Clinical and Laboratory Standards Institute. M100: Performance Standards for Antimicrobial Susceptibility Testing 30th edn, 1–320 (CLSI, 2020).
Wick, R. R., Judd, L. M., Gorrie, C. L. & Holt, K. E. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13, e1005595 (2017).
pubmed: 28594827 pmcid: 5481147 doi: 10.1371/journal.pcbi.1005595
Andrews, S. FastQC https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2012).
Ewels, P., Magnusson, M., Lundin, S. & Käller, M. MultiQC: Summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047–3048 (2016).
pubmed: 27312411 pmcid: 5039924 doi: 10.1093/bioinformatics/btw354
Deatherage, D. E. & Barrick, J. E. Engineering and Analyzing Multicellular Systems (Springer, 2014).
Cafini, F. et al. Methodology for the study of horizontal gene transfer in Staphylococcus aureus. JoVE (J. Vis. Exp.) 121, e55087 (2017).
Ruiz‐Ripa, L. et al. Linezolid‐resistant MRSA‐CC398 carrying the cfr gene, and MRSA‐CC9 isolates from pigs with signs of infection in Spain. J. Appl. Microbiol. 131, 615–622 (2021).
pubmed: 33386630 doi: 10.1111/jam.14988
Kehrenberg, C. & Schwarz, S. Distribution of florfenicol resistance genes fexA and cfr among chloramphenicol-resistant Staphylococcus isolates. Antimicrobial Agents Chemother. 50, 1156–1163 (2006).
doi: 10.1128/AAC.50.4.1156-1163.2006

Auteurs

Zhengan Wang (Z)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Chao Gu (C)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Department of Respiratory Medicine, The First Hospital of Jiaxing (the Affiliated Hospital of Jiaxing University), 1882 South Zhonghuan Road, Jiaxing, Zhejiang Province, China.

Lu Sun (L)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Feng Zhao (F)

Department of Clinical Laboratory, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang Province, China.
Key Laboratory of Precision Medicine in Diagnosis and Monitoring Research of Zhejiang Province, Hangzhou, Zhejiang Province, China.

Ying Fu (Y)

Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Department of Clinical Laboratory, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang Province, China.
Key Laboratory of Precision Medicine in Diagnosis and Monitoring Research of Zhejiang Province, Hangzhou, Zhejiang Province, China.

Lingfang Di (L)

Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Department of Clinical Laboratory, Tongxiang First people's hospital, Tongxiang, Zhejiang Province, China.

Junxiong Zhang (J)

Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Department of Clinical Laboratory, Linping Traditional Chinese Medicine Hospital, Hangzhou, China.

Hemu Zhuang (H)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Shengnan Jiang (S)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Haiping Wang (H)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Feiteng Zhu (F)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Yiyi Chen (Y)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Mengzhen Chen (M)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Xia Ling (X)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.
Blood center of Zhejiang province, Hangzhou, Zhejiang Province, China.

Yan Chen (Y)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China. chenyan@zju.edu.cn.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China. chenyan@zju.edu.cn.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China. chenyan@zju.edu.cn.

Yunsong Yu (Y)

Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China. yvys119@zju.edu.cn.
Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang Province, China. yvys119@zju.edu.cn.
Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China. yvys119@zju.edu.cn.

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