Identification and characterization of mutations responsible for the β-lactam resistance in oxacillin-susceptible mecA-positive Staphylococcus aureus.
Anti-Bacterial Agents
/ pharmacology
Bacterial Proteins
/ genetics
DNA-Directed RNA Polymerases
/ genetics
Down-Regulation
/ drug effects
Gene Expression Regulation, Bacterial
/ drug effects
Genome
/ genetics
Genome-Wide Association Study
/ methods
Humans
Microbial Sensitivity Tests
/ methods
Mutation
/ genetics
Oxacillin
/ pharmacology
Phylogeny
Staphylococcal Infections
/ drug therapy
Staphylococcus aureus
/ drug effects
Transcription, Genetic
/ drug effects
Up-Regulation
/ drug effects
beta-Lactam Resistance
/ genetics
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 10 2020
09 10 2020
Historique:
received:
04
03
2020
accepted:
20
09
2020
entrez:
10
10
2020
pubmed:
11
10
2020
medline:
13
1
2021
Statut:
epublish
Résumé
Staphylococcus aureus strains that are susceptible to the β-lactam antibiotic oxacillin despite carrying mecA (OS-MRSA) cause serious clinical problems globally because of their ability to easily acquire β-lactam resistance. Understanding the genetic mechanism(s) of acquisition of the resistance is therefore crucial for infection control management. For this purpose, a whole-genome sequencing-based analysis was performed using 43 clinical OS-MRSA strains and 100 mutants with reduced susceptibility to oxacillin (MICs 1.0-256 µg/mL) generated from 26 representative OS-MRSA strains. Genome comparison between the mutants and their respective parent strains identified a total of 141 mutations in 46 genes and 8 intergenic regions. Among them, the mutations are frequently found in genes related to RNA polymerase (rpoBC), purine biosynthesis (guaA, prs, hprT), (p)ppGpp synthesis (rel
Identifiants
pubmed: 33037239
doi: 10.1038/s41598-020-73796-5
pii: 10.1038/s41598-020-73796-5
pmc: PMC7547103
doi:
Substances chimiques
Anti-Bacterial Agents
0
Bacterial Proteins
0
DNA-Directed RNA Polymerases
EC 2.7.7.6
Oxacillin
UH95VD7V76
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
16907Références
Gordon, R. J. & Lowy, F. D. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin. Infect. Dis. 46(Suppl 5), S350-359. https://doi.org/10.1086/533591 (2008).
doi: 10.1086/533591
pubmed: 18462090
pmcid: 2474459
Fluit, A. C. Livestock-associated Staphylococcus aureus. Clin. Microbiol. Infect. 18, 735–744. https://doi.org/10.1111/j.1469-0691.2012.03846.x (2012).
doi: 10.1111/j.1469-0691.2012.03846.x
pubmed: 22512702
Stapleton, P. D. & Taylor, P. W. Methicillin resistance in Staphylococcus aureus: Mechanisms and modulation. Sci. Prog. 85, 57–72. https://doi.org/10.3184/003685002783238870 (2002).
doi: 10.3184/003685002783238870
pubmed: 11969119
pmcid: 2065735
Boucher, H. W. & Corey, G. R. Epidemiology of methicillin-resistant Staphylococcus aureus. Clin. Infect. Dis. 46(Suppl 5), S344-349. https://doi.org/10.1086/533590 (2008).
doi: 10.1086/533590
pubmed: 18462089
Cuny, C., Wieler, L. H. & Witte, W. Livestock-associated MRSA: The impact on humans. Antibiotics (Basel) 4, 521–543. https://doi.org/10.3390/antibiotics4040521 (2015).
doi: 10.3390/antibiotics4040521
Foster, T. J. Antibiotic resistance in Staphylococcus aureus. Current status and future prospects. FEMS Microbiol Rev 41, 430–449. https://doi.org/10.1093/femsre/fux007 (2017).
doi: 10.1093/femsre/fux007
pubmed: 28419231
Llarrull, L. I., Fisher, J. F. & Mobashery, S. Molecular basis and phenotype of methicillin resistance in Staphylococcus aureus and insights into new beta-lactams that meet the challenge. Antimicrob. Agents Chemother. 53, 4051–4063. https://doi.org/10.1128/AAC.00084-09 (2009).
doi: 10.1128/AAC.00084-09
pubmed: 19470504
pmcid: 2764218
Fuda, C. C., Fisher, J. F. & Mobashery, S. Beta-lactam resistance in Staphylococcus aureus: The adaptive resistance of a plastic genome. Cell Mol. Life Sci. 62, 2617–2633. https://doi.org/10.1007/s00018-005-5148-6 (2005).
doi: 10.1007/s00018-005-5148-6
pubmed: 16143832
Mistry, H. et al. Prevalence and characterization of oxacillin susceptible mecA-positive clinical isolates of Staphylococcus aureus causing bovine mastitis in India. PLoS ONE 11, e0162256. https://doi.org/10.1371/journal.pone.0162256 (2016).
doi: 10.1371/journal.pone.0162256
pubmed: 27603123
pmcid: 5014444
Saeed, K. et al. Oxacillin-susceptible methicillin-resistant Staphylococcus aureus (OS-MRSA), a hidden resistant mechanism among clinically significant isolates in the Wessex region/UK. Infection 42, 843–847. https://doi.org/10.1007/s15010-014-0641-1 (2014).
doi: 10.1007/s15010-014-0641-1
pubmed: 24919530
Andrade-Figueiredo, M. & Leal-Balbino, T. C. Clonal diversity and epidemiological characteristics of Staphylococcus aureus: High prevalence of oxacillin-susceptible mecA-positive Staphylococcus aureus (OS-MRSA) associated with clinical isolates in Brazil. BMC Microbiol. 16, 115. https://doi.org/10.1186/s12866-016-0733-4 (2016).
doi: 10.1186/s12866-016-0733-4
pubmed: 27325108
pmcid: 4915036
Song, Y., Cui, L., Lv, Y., Li, Y. & Xue, F. Characterisation of clinical isolates of oxacillin-susceptible mecA-positive Staphylococcus aureus in China from 2009 to 2014. J. Glob. Antimicrob. Resist. 11, 1–3. https://doi.org/10.1016/j.jgar.2017.05.009 (2017).
doi: 10.1016/j.jgar.2017.05.009
pubmed: 28729204
Quijada, N. M. et al. Oxacillin-susceptible mecA-positive Staphylococcus aureus associated with processed food in Europe. Food Microbiol. 82, 107–110. https://doi.org/10.1016/j.fm.2019.01.021 (2019).
doi: 10.1016/j.fm.2019.01.021
pubmed: 31027762
Conceição, T., Coelho, C., de Lencastre, H. & Aires-de-Sousa, M. Frequent occurrence of oxacillin-susceptible mecA-positive Staphylococcus aureus (OS-MRSA) strains in two African countries. J. Antimicrob. Chemother. 70, 3200–3204. https://doi.org/10.1093/jac/dkv261 (2015).
doi: 10.1093/jac/dkv261
pubmed: 26318189
Hososaka, Y. et al. Characterization of oxacillin-susceptible mecA-positive Staphylococcus aureus: A new type of MRSA. J. Infect. Chemother. 13, 79–86. https://doi.org/10.1007/s10156-006-0502-7 (2007).
doi: 10.1007/s10156-006-0502-7
pubmed: 17458674
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-three Informational Supplement M100-S23. CLSI, Wayne, PA, USA, 2013.
Pu, W. et al. High incidence of oxacillin-susceptible mecA-positive Staphylococcus aureus (OS-MRSA) associated with bovine mastitis in China. PLoS ONE 9, e88134. https://doi.org/10.1371/journal.pone.0088134 (2014).
doi: 10.1371/journal.pone.0088134
pubmed: 24523877
pmcid: 3921137
Sakoulas, G. et al. Methicillin-resistant Staphylococcus aureus: comparison of susceptibility testing methods and analysis of mecA-positive susceptible strains. J. Clin. Microbiol. 39, 3946–3951. https://doi.org/10.1128/JCM.39.11.3946-3951.2001 (2001).
doi: 10.1128/JCM.39.11.3946-3951.2001
pubmed: 11682512
pmcid: 88469
Ikonomidis, A. et al. In vitro and in vivo evaluations of oxacillin efficiency against mecA-positive oxacillin-susceptible Staphylococcus aureus. Antimicrob. Agents Chemother. 52, 3905–3908. https://doi.org/10.1128/AAC.00653-08 (2008).
doi: 10.1128/AAC.00653-08
pubmed: 18694946
pmcid: 2573153
Duarte, F. C. et al. Fatal sepsis caused by mecA-positive oxacillin-susceptible Staphylococcus aureus: First report in a tertiary hospital of southern Brazil. J. Infect. Chemother. 25, 293–297. https://doi.org/10.1016/j.jiac.2018.09.010 (2019).
doi: 10.1016/j.jiac.2018.09.010
pubmed: 30482697
Goering, R. V., Swartzendruber, E. A., Obradovich, A. E., Tickler, I. A. & Tenover, F. C. Emergence of oxacillin resistance in stealth methicillin-resistant. Antimicrob. Agents Chemother. 63, e00558-e619. https://doi.org/10.1128/AAC.00558-19 (2019).
doi: 10.1128/AAC.00558-19
pubmed: 31109981
pmcid: 6658785
Chung, M. et al. Heterogeneous oxacillin-resistant phenotypes and production of PBP2A by oxacillin-susceptible/mecA-positive MRSA strains from Africa. J. Antimicrob. Chemother. 71, 2804–2809. https://doi.org/10.1093/jac/dkw209 (2016).
doi: 10.1093/jac/dkw209
pubmed: 27278899
pmcid: 5031915
Gratani, F. L. et al. Regulation of the opposing (p)ppGpp synthetase and hydrolase activities in a bifunctional RelA/SpoT homologue from Staphylococcus aureus. PLoS Genet. 14, e1007514. https://doi.org/10.1371/journal.pgen.1007514 (2018).
doi: 10.1371/journal.pgen.1007514
pubmed: 29985927
pmcid: 6053245
Ender, M., McCallum, N. & Berger-Bächi, B. Impact of mecA promoter mutations on mecA expression and beta-lactam resistance levels. Int. J. Med. Microbiol. 298, 607–617. https://doi.org/10.1016/j.ijmm.2008.01.015 (2008).
doi: 10.1016/j.ijmm.2008.01.015
pubmed: 18456552
Kuroda, M. et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357, 1225–1240. https://doi.org/10.1016/s0140-6736(00)04403-2 (2001).
doi: 10.1016/s0140-6736(00)04403-2
pubmed: 11418146
Liu, P., Xue, H., Wu, Z., Ma, J. & Zhao, X. Effect of bla regulators on the susceptible phenotype and phenotypic conversion for oxacillin-susceptible mecA-positive staphylococcal isolates. J. Antimicrob. Chemother. 71, 2105–2112. https://doi.org/10.1093/jac/dkw123 (2016).
doi: 10.1093/jac/dkw123
pubmed: 27154864
Geiger, T. et al. The stringent response of Staphylococcus aureus and its impact on survival after phagocytosis through the induction of intracellular PSMs expression. PLoS Pathog. 8, e1003016. https://doi.org/10.1371/journal.ppat.1003016 (2012).
doi: 10.1371/journal.ppat.1003016
pubmed: 23209405
pmcid: 3510239
Geiger, T. et al. Role of the (p)ppGpp synthase RSH, a RelA/SpoT homolog, in stringent response and virulence of Staphylococcus aureus. Infect. Immun. 78, 1873–1883. https://doi.org/10.1128/IAI.01439-09 (2010).
doi: 10.1128/IAI.01439-09
pubmed: 20212088
pmcid: 2863498
Steiner, K. & Malke, H. relA-Independent amino acid starvation response network of Streptococcus pyogenes. J. Bacteriol. 183, 7354–7364. https://doi.org/10.1128/JB.183.24.7354-7364.2001 (2001).
doi: 10.1128/JB.183.24.7354-7364.2001
pubmed: 11717294
pmcid: 95584
Bæk, K. T. et al. β-Lactam resistance in methicillin-resistant Staphylococcus aureus USA300 is increased by inactivation of the ClpXP protease. Antimicrob. Agents Chemother. 58, 4593–4603. https://doi.org/10.1128/AAC.02802-14 (2014).
doi: 10.1128/AAC.02802-14
pubmed: 24867990
pmcid: 4136064
Dordel, J. et al. Novel determinants of antibiotic resistance: identification of mutated loci in highly methicillin-resistant subpopulations of methicillin-resistant Staphylococcus aureus. MBio 5, e01000. https://doi.org/10.1128/mBio.01000-13 (2014).
doi: 10.1128/mBio.01000-13
pubmed: 24713324
pmcid: 3993859
Kim, C. et al. The mechanism of heterogeneous beta-lactam resistance in MRSA: Key role of the stringent stress response. PLoS ONE 8, e82814. https://doi.org/10.1371/journal.pone.0082814 (2013).
doi: 10.1371/journal.pone.0082814
pubmed: 24349368
pmcid: 3857269
Pardos de la Gandara, M. et al. Genetic determinants of high-level oxacillin resistance in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents. Chemother. 62, e00206-18. https://doi.org/10.1128/AAC.00206-18 (2018).
doi: 10.1128/AAC.00206-18
pubmed: 29555636
pmcid: 5971597
Aedo, S. & Tomasz, A. Role of the stringent stress response in the antibiotic resistance phenotype of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 60, 2311–2317. https://doi.org/10.1128/AAC.02697-15 (2016).
doi: 10.1128/AAC.02697-15
pubmed: 26833147
pmcid: 4808156
Bui, L. M., Conlon, B. P. & Kidd, S. P. Antibiotic tolerance and the alternative lifestyles of. Essays Biochem. 61, 71–79. https://doi.org/10.1042/EBC20160061 (2017).
doi: 10.1042/EBC20160061
pubmed: 28258231
Onyango, L. A. & Alreshidi, M. M. Adaptive metabolism in staphylococci: Survival and persistence in environmental and clinical settings. J. Pathog. 2018, 1092632. https://doi.org/10.1155/2018/1092632 (2018).
doi: 10.1155/2018/1092632
pubmed: 30327733
pmcid: 6171259
Cassels, R., Oliva, B. & Knowles, D. Occurrence of the regulatory nucleotides ppGpp and pppGpp following induction of the stringent response in staphylococci. J. Bacteriol. 177, 5161–5165. https://doi.org/10.1128/jb.177.17.5161-5165.1995 (1995).
doi: 10.1128/jb.177.17.5161-5165.1995
pubmed: 7665499
pmcid: 177300
Murakami, K. et al. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J. Clin. Microbiol. 29, 2240–2244 (1991).
doi: 10.1128/JCM.29.10.2240-2244.1991
Hiramatsu, K., Kihara, H. & Yokota, T. Analysis of borderline-resistant strains of methicillin-resistant Staphylococcus aureus using polymerase chain reaction. Microbiol. Immunol. 36, 445–453. https://doi.org/10.1111/j.1348-0421.1992.tb02043.x (1992).
doi: 10.1111/j.1348-0421.1992.tb02043.x
pubmed: 1513261
Kampf, G., Adena, S., Rüden, H. & Weist, K. Inducibility and potential role of MecA-gene-positive oxacillin-susceptible Staphylococcus aureus from colonized healthcare workers as a source for nosocomial infections. J. Hosp. Infect. 54, 124–129. https://doi.org/10.1016/s0195-6701(03)00119-1 (2003).
doi: 10.1016/s0195-6701(03)00119-1
pubmed: 12818586
Phaku, P. et al. Unveiling the molecular basis of antimicrobial resistance in Staphylococcus aureus from the Democratic Republic of the Congo using whole genome sequencing. Clin. Microbiol. Infect. 22(644), e641-645. https://doi.org/10.1016/j.cmi.2016.04.009 (2016).
doi: 10.1016/j.cmi.2016.04.009
Roisin, S., Nonhoff, C., Denis, O. & Struelens, M. J. Evaluation of new Vitek 2 card and disk diffusion method for determining susceptibility of Staphylococcus aureus to oxacillin. J. Clin. Microbiol. 46, 2525–2528. https://doi.org/10.1128/JCM.00291-08 (2008).
doi: 10.1128/JCM.00291-08
pubmed: 18550733
pmcid: 2519473
Sharma, S., Srivastava, P., Kulshrestha, A. & Abbas, A. Evaluation of different phenotypic methods for the detection of methicillin resistant Staphylococcus aureus and antimicrobial susceptibility pattern of MRSA. Int. J. Community Med. Public Health 4(9), 3297–3301 (2017). https://doi.org/10.18203/2394-6040.ijcmph20173832 .
doi: 10.18203/2394-6040.ijcmph20173832
Proulx, M. K. et al. Reversion from methicillin susceptibility to methicillin resistance in Staphylococcus aureus during treatment of bacteremia. J. Infect. Dis. 213, 1041–1048. https://doi.org/10.1093/infdis/jiv512 (2016).
doi: 10.1093/infdis/jiv512
pubmed: 26503983
Chen, F. J., Wang, C. H., Chen, C. Y., Hsu, Y. C. & Wang, K. T. Role of the mecA gene in oxacillin resistance in a Staphylococcus aureus clinical strain with a pvl-positive ST59 genetic background. Antimicrob. Agents Chemother. 58, 1047–1054. https://doi.org/10.1128/AAC.02045-13 (2014).
doi: 10.1128/AAC.02045-13
pubmed: 24277044
pmcid: 3910894
McKinney, T. K., Sharma, V. K., Craig, W. A. & Archer, G. L. Transcription of the gene mediating methicillin resistance in Staphylococcus aureus (mecA) is corepressed but not coinduced by cognate mecA and beta-lactamase regulators. J. Bacteriol. 183, 6862–6868. https://doi.org/10.1128/JB.183.23.6862-6868.2001 (2001).
doi: 10.1128/JB.183.23.6862-6868.2001
pubmed: 11698375
pmcid: 95527
Mwangi, M. M. et al. Whole-genome sequencing reveals a link between β-lactam resistance and synthetases of the alarmone (p)ppGpp in Staphylococcus aureus. Microb. Drug Resist. 19, 153–159. https://doi.org/10.1089/mdr.2013.0053 (2013).
doi: 10.1089/mdr.2013.0053
pubmed: 23659600
pmcid: 3662374
Anderson, K. L. et al. Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J. Bacteriol. 188, 6739–6756. https://doi.org/10.1128/JB.00609-06 (2006).
doi: 10.1128/JB.00609-06
pubmed: 16980476
pmcid: 1595530
Hughes, J. & Mellows, G. On the mode of action of pseudomonic acid: Inhibition of protein synthesis in Staphylococcus aureus. J. Antibiot. (Tokyo) 31, 330–335. https://doi.org/10.7164/antibiotics.31.330 (1978).
doi: 10.7164/antibiotics.31.330
Haseltine, W. A. & Block, R. Synthesis of guanosine tetra- and pentaphosphate requires the presence of a codon-specific, uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc. Natl. Acad. Sci. USA 70, 1564–1568. https://doi.org/10.1073/pnas.70.5.1564 (1973).
doi: 10.1073/pnas.70.5.1564
pubmed: 4576025
Liu, K., Bittner, A. N. & Wang, J. D. Diversity in (p)ppGpp metabolism and effectors. Curr. Opin. Microbiol. 24, 72–79. https://doi.org/10.1016/j.mib.2015.01.012 (2015).
doi: 10.1016/j.mib.2015.01.012
pubmed: 25636134
pmcid: 4380541
Hauryliuk, V., Atkinson, G. C., Murakami, K. S., Tenson, T. & Gerdes, K. Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat. Rev. Microbiol. 13, 298–309. https://doi.org/10.1038/nrmicro3448 (2015).
doi: 10.1038/nrmicro3448
pubmed: 25853779
pmcid: 4659695
Aiba, Y. et al. Mutation of RNA polymerase β-subunit gene promotes heterogeneous-to-homogeneous conversion of β-lactam resistance in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 57, 4861–4871. https://doi.org/10.1128/AAC.00720-13 (2013).
doi: 10.1128/AAC.00720-13
pubmed: 23877693
pmcid: 3811421
Matsuo, M., Yamamoto, N., Hishinuma, T. & Hiramatsu, K. Identification of a novel gene associated with high-level β-Lactam resistance in heterogeneous vancomycin-intermediate Staphylococcus aureus strain Mu3 and methicillin-resistant S. aureus Strain N315. Antimicrob. Agents Chemother.63, e00712-18, https://doi.org/10.1128/AAC.00712-18 (2019).
Thalsø-Madsen, I. et al. The Sle1 Cell wall amidase is essential for β-Lactam resistance in community acquired methicillin resistant. Antimicrob. Agents Chemother. 64, e01931-e2019. https://doi.org/10.1128/AAC.01931-19 (2019).
doi: 10.1128/AAC.01931-19
pubmed: 31685469
pmcid: 7187620
Andersson, D. I. & Hughes, D. Antibiotic resistance and its cost: Is it possible to reverse resistance?. Nat. Rev. Microbiol. 8, 260–271. https://doi.org/10.1038/nrmicro2319 (2010).
doi: 10.1038/nrmicro2319
pubmed: 20208551
Baumert, N. et al. Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb. Drug Resist. 8, 253–260. https://doi.org/10.1089/10766290260469507 (2002).
doi: 10.1089/10766290260469507
pubmed: 12523621
Chuard, C., Vaudaux, P. E., Proctor, R. A. & Lew, D. P. Decreased susceptibility to antibiotic killing of a stable small colony variant of Staphylococcus aureus in fluid phase and on fibronectin-coated surfaces. J. Antimicrob. Chemother. 39, 603–608. https://doi.org/10.1093/jac/39.5.603 (1997).
doi: 10.1093/jac/39.5.603
pubmed: 9184359
Garcia, L. G. et al. Antibiotic activity against small-colony variants of Staphylococcus aureus: Review of in vitro, animal and clinical data. J. Antimicrob. Chemother. 68, 1455–1464. https://doi.org/10.1093/jac/dkt072 (2013).
doi: 10.1093/jac/dkt072
pubmed: 23485724
Cui, L., Neoh, H. M., Iwamoto, A. & Hiramatsu, K. Coordinated phenotype switching with large-scale chromosome flip-flop inversion observed in bacteria. Proc. Natl. Acad. Sci. USA 109, E1647-1656. https://doi.org/10.1073/pnas.1204307109 (2012).
doi: 10.1073/pnas.1204307109
pubmed: 22645353
Saito, M. et al. “Slow VISA,” a novel phenotype of vancomycin resistance, found in vitro in heterogeneous vancomycin-intermediate Staphylococcus aureus strain Mu3. Antimicrob. Agents Chemother. 58, 5024–5035. https://doi.org/10.1128/AAC.02470-13 (2014).
doi: 10.1128/AAC.02470-13
pubmed: 24841271
pmcid: 4135821
Katayama, Y. et al. Prevalence of slow-growth vancomycin nonsusceptibility in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 61, e00452-e517. https://doi.org/10.1128/AAC.00452-17 (2017).
doi: 10.1128/AAC.00452-17
pubmed: 28827421
pmcid: 5655046
Kanesaka, I. et al. Characterization of compensatory mutations associated with restoration of daptomycin-susceptibility in daptomycin non-susceptible methicillin-resistant Staphylococcus aureus and the role mprF mutations. J. Infect. Chemother. 25, 1–5. https://doi.org/10.1016/j.jiac.2018.09.009 (2019).
doi: 10.1016/j.jiac.2018.09.009
pubmed: 30322736
Wada, A. et al. Ratio of mecA gene in oxacillin-insusceptible and susceptible Staphylococcus aureus. Jpn. J. Chemother. 55(5), 374–377 (2007).
Chen, F. J. et al. mecA-positive Staphylococcus aureus with low-level oxacillin MIC in Taiwan. J. Clin. Microbiol. 50, 1679–1683. https://doi.org/10.1128/JCM.06711-11 (2012).
doi: 10.1128/JCM.06711-11
pubmed: 22378906
pmcid: 3347131
Watanabe, S. et al. Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis. BMC Genomics 19, 810. https://doi.org/10.1186/s12864-018-5185-9 (2018).
doi: 10.1186/s12864-018-5185-9
pubmed: 30409159
pmcid: 6225691
Watanabe, S. et al. Complete genome sequence of streptococcus pyogenes Strain JMUB1235 isolated from an acute phlegmonous gastritis patient. Genome Announc. 4, e01133-e1216. https://doi.org/10.1128/genomeA.01133-16 (2016).
doi: 10.1128/genomeA.01133-16
pubmed: 27795272
pmcid: 5073259
Watanabe, S. et al. Composition and diversity of CRISPR-Cas13a systems in the genus Leptotrichia. Front. Microbiol. 10, 2838. https://doi.org/10.3389/fmicb.2019.02838 (2019).
doi: 10.3389/fmicb.2019.02838
pubmed: 31921024
pmcid: 6914741
Gardner, S. N., Slezak, T. & Hall, B. G. kSNP3.0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome. Bioinformatics 31, 2877–2878. https://doi.org/10.1093/bioinformatics/btv271 (2015).
doi: 10.1093/bioinformatics/btv271
pubmed: 25913206
Neoh, H. M. et al. Mutated response regulator graR is responsible for phenotypic conversion of Staphylococcus aureus from heterogeneous vancomycin-intermediate resistance to vancomycin-intermediate resistance. Antimicrob. Agents Chemother. 52, 45–53. https://doi.org/10.1128/AAC.00534-07 (2008).
doi: 10.1128/AAC.00534-07
pubmed: 17954695
Kato, F. & Sugai, M. A simple method of markerless gene deletion in Staphylococcus aureus. J. Microbiol. Methods 87, 76–81. https://doi.org/10.1016/j.mimet.2011.07.010 (2011).
doi: 10.1016/j.mimet.2011.07.010
pubmed: 21801759
Sato’o, Y. et al. Optimized universal protocol for electroporation of both coagulase-positive and -negative Staphylococci. J. Microbiol. Methods 146, 25–32. https://doi.org/10.1016/j.mimet.2018.01.006 (2018).
doi: 10.1016/j.mimet.2018.01.006
pubmed: 29355575