{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T18:18:37Z","timestamp":1787163517074,"version":"build-2736575974"},"reference-count":67,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2022,4,8]],"date-time":"2022-04-08T00:00:00Z","timestamp":1649376000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004681","name":"Higher Education Commission","doi-asserted-by":"publisher","award":["4774"],"award-info":[{"award-number":["4774"]}],"id":[{"id":"10.13039\/501100004681","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002383","name":"King Saud University","doi-asserted-by":"publisher","award":["RSP2022R491"],"award-info":[{"award-number":["RSP2022R491"]}],"id":[{"id":"10.13039\/501100002383","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Staphylococcus aureus (S. aureus) ST22 is considered a clinically important clone because an epidemic strain EMRSA-15 belongs to ST22, and several outbreaks of this clone have been documented worldwide. We performed genomic analysis of an S. aureus strain Lr2 ST22 from Pakistan and determined comparative analysis with other ST22 strains. The genomic data show that Lr2 belongs to spa-type t2986 and harbors staphylococcal cassette chromosome mec (SCCmec) type IVa(2B), one complete plasmid, and seven prophages or prophage-like elements. The strain harbors several prophage-associated virulence factors, including Panton\u2013Valentine leukocidin (PVL) and toxic shock syndrome toxin (TSST). The single nucleotide polymorphism (SNPs)-based phylogenetic relationship inferred from whole genome and core genome revealed that strain Lr2 exhibits the nearest identities to a South African community-acquired methicillin-resistant S. aureus (CA-MRSA) ST22 strain and makes a separate clade with an Indian CA-MRSA ST22 strain. Although most ST22 strains carry blaZ, mecA, and mutations in gyrA, the Lr2 strain does not have the blaZ gene but, unlike other ST22 strains, carries the antibiotic resistance genes erm(C) and aac(6\u2032)-Ie-aph(2\u2033)-Ia. Among ST22 strains analyzed, only the strain Lr2 possesses both PVL and TSST genes. The functional annotation of genes unique to Lr2 revealed that mobilome is the third-largest Cluster of Orthologous Genes (COGs) category, which encodes genes associated with prophages and transposons. This possibly makes methicillin-resistant S. aureus (MRSA) Lr2 ST22 strain highly virulent, and this study would improve the knowledge of MRSA ST22 strains in Pakistan. However, further studies are needed on a large collection of MRSA to comprehend the genomic epidemiology and evolution of this clone in Pakistan.<\/jats:p>","DOI":"10.3390\/antibiotics11040496","type":"journal-article","created":{"date-parts":[[2022,4,8]],"date-time":"2022-04-08T12:11:14Z","timestamp":1649419874000},"page":"496","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Comparative Genomic Analysis of a Panton\u2013Valentine Leukocidin-Positive ST22 Community-Acquired Methicillin-Resistant Staphylococcus aureus from Pakistan"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7138-1272","authenticated-orcid":false,"given":"Nimat","family":"Ullah","sequence":"first","affiliation":[{"name":"Atta-ur-Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), Sector H-12, Islamabad 44000, Pakistan"},{"name":"Department of Microbiology and Immunology, Indiana University School of Medicine-Northwest, 3400 Broadway, Gary, IN 46408, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samavi","family":"Nasir","sequence":"additional","affiliation":[{"name":"Atta-ur-Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), Sector H-12, Islamabad 44000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6140-2861","authenticated-orcid":false,"given":"Zaara","family":"Ishaq","sequence":"additional","affiliation":[{"name":"Atta-ur-Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), Sector H-12, Islamabad 44000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8792-8471","authenticated-orcid":false,"given":"Farha","family":"Anwer","sequence":"additional","affiliation":[{"name":"Atta-ur-Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), Sector H-12, Islamabad 44000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tanzeela","family":"Raza","sequence":"additional","affiliation":[{"name":"Atta-ur-Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), Sector H-12, Islamabad 44000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Moazur","family":"Rahman","sequence":"additional","affiliation":[{"name":"School of Biological Sciences, University of the Punjab, Quaid-i-Azam Campus, Lahore 54590, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abdulrahman","family":"Alshammari","sequence":"additional","affiliation":[{"name":"Department of Pharmacology and Toxicology, College of Pharmacy, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Metab","family":"Alharbi","sequence":"additional","affiliation":[{"name":"Department of Pharmacology and Toxicology, College of Pharmacy, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0576-2851","authenticated-orcid":false,"given":"Taeok","family":"Bae","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Indiana University School of Medicine-Northwest, 3400 Broadway, Gary, IN 46408, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0393-5384","authenticated-orcid":false,"given":"Abdur","family":"Rahman","sequence":"additional","affiliation":[{"name":"Atta-ur-Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), Sector H-12, Islamabad 44000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0486-4661","authenticated-orcid":false,"given":"Amjad","family":"Ali","sequence":"additional","affiliation":[{"name":"Atta-ur-Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), Sector H-12, Islamabad 44000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,4,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1128\/JCM.01867-09","article-title":"Molecular Characterization of Methicillin-Resistant Staphylococcus aureus with Emergence of Epidemic Clones of Sequence Type (ST) 22 and ST 772 in Mumbai, India","volume":"48","author":"Rodrigues","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_2","unstructured":"Taylor, T.A., and Unakal, C.G. (2017). Staphylococcus Aureus, StatPearls Publishing."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Mitevska, E., Wong, B., Surewaard, B.G.J., and Jenne, C.N. (2021). The Prevalence, Risk, and Management of Methicillin-Resistant Staphylococcus aureus Infection in Diverse Populations across Canada: A Systematic Review. Pathogens, 10.","DOI":"10.3390\/pathogens10040393"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Yeo, W.-S., Jeong, B., Ullah, N., Shah, M.A., Ali, A., Kim, K.K., and Bae, T. (2021). Ftsh Sensitizes Methicillin-Resistant Staphylococcus aureus to \u03b2-Lactam Antibiotics by Degrading YpfP, a Lipoteichoic Acid Synthesis Enzyme. Antibiotics, 10.","DOI":"10.3390\/antibiotics10101198"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2842","DOI":"10.1128\/JCM.00521-08","article-title":"Molecular epidemiology of methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from global clinical trials","volume":"46","author":"Goering","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"101539","DOI":"10.1016\/j.bjid.2021.101539","article-title":"Community-genotype methicillin-resistant Staphylococcus aureus skin and soft tissue infections in Latin America: A systematic review","volume":"25","author":"Leme","year":"2021","journal-title":"Braz. J. Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"521","DOI":"10.3390\/antibiotics4040521","article-title":"Livestock-associated MRSA: The impact on humans","volume":"4","author":"Cuny","year":"2015","journal-title":"Antibiotics"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2921","DOI":"10.2147\/IDR.S262123","article-title":"Two Cases of Intrafamilial Transmission of Community-Acquired Methicillin-Resistant Staphylococcus aureus Producing Both PVL and TSST-1 Causing Fatal Necrotizing Pneumonia and Sepsis","volume":"13","author":"Hayakawa","year":"2020","journal-title":"Infect. Drug Resist."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"684","DOI":"10.1128\/JCM.01917-10","article-title":"Distinct bacteriophages encoding Panton-Valentine leukocidin (PVL) among international methicillin-resistant Staphylococcus aureus clones harboring PVL","volume":"49","author":"Boakes","year":"2011","journal-title":"J. Clin. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"978","DOI":"10.3201\/eid0908.030089","article-title":"Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: Worldwide emergence","volume":"9","author":"Vandenesch","year":"2003","journal-title":"Emerg. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.nmni.2016.02.001","article-title":"Detection of ST772 Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus (Bengal Bay clone) and ST22 S. aureus isolates with a genetic variant of elastin binding protein in Nepal","volume":"11","author":"Pokhrel","year":"2016","journal-title":"New Microbes New Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1016\/S0140-6736(09)61999-1","article-title":"Community-associated meticillin-resistant Staphylococcus aureus","volume":"375","author":"DeLeo","year":"2010","journal-title":"Lancet"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1128\/JCM.44.1.108-118.2006","article-title":"Characterization of a Strain of Community-Associated Methicillin-Resistant Staphylococcus aureus Widely Disseminated in the UnitedStates","volume":"44","author":"Tenover","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1128\/AAC.01001-07","article-title":"Novel characteristics of community-acquired methicillin-resistant Staphylococcus aureus strains belonging to multilocus sequence type 59 in Taiwan","volume":"52","author":"Takano","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"4077","DOI":"10.1128\/AAC.00847-06","article-title":"Molecular characteristics and in vitro susceptibility to antimicrobial agents, including the des-fluoro (6) quinolone DX-619, of Panton-Valentine leucocidin-positive methicillin-resistant Staphylococcus aureus isolates from the community and hospitals","volume":"50","author":"Yamamoto","year":"2006","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"106264","DOI":"10.1016\/j.ijantimicag.2020.106264","article-title":"Comparative genome analysis of global and Russian strains of community-acquired methicillin-resistant Staphylococcus aureus ST22, a \u2018Gaza clone\u2019","volume":"57","author":"Gostev","year":"2021","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1101\/gr.196709.115","article-title":"Building a genomic framework for prospective MRSA surveillance in the United Kingdom and the Republic of Ireland","volume":"26","author":"Reuter","year":"2016","journal-title":"Genome Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1101\/gr.147710.112","article-title":"A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic","volume":"23","author":"Holden","year":"2013","journal-title":"Genome Res."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Khan, S., Marasa, B.S., Sung, K., and Nawaz, M. (2021). Genotypic Characterization of Clinical Isolates of\u00a0Staphylococcus aureus from Pakistan. Pathogens, 10.","DOI":"10.3390\/pathogens10080918"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Ullah, N., Dar, H.A., Naz, K., Andleeb, S., Rahman, A., Saeed, M.T., Hanan, F., Bae, T., and Ali, A.J.A. (2021). Genomic Investigation of Methicillin-Resistant Staphylococcus aureus ST113 Strains Isolated from Tertiary Care Hospitals in Pakistan. Antibiotics, 10.","DOI":"10.3390\/antibiotics10091121"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.jgar.2019.09.015","article-title":"Whole-genome sequencing of a new sequence type (ST5352) strain of community-acquired methicillin-resistant Staphylococcus aureus from a hospital in Pakistan","volume":"19","author":"Ullah","year":"2019","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e10185","DOI":"10.7717\/peerj.10185","article-title":"Genome-wide comparison of four MRSA clinical isolates from Germany and Hungary","volume":"9","author":"Naorem","year":"2021","journal-title":"PeerJ"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1186\/s40246-015-0037-z","article-title":"Whole-genome sequencing targets drug-resistant bacterial infections","volume":"9","author":"Punina","year":"2015","journal-title":"Hum. Genom."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1700592","DOI":"10.2807\/1560-7917.ES.2018.23.34.1700592","article-title":"Genomic epidemiology of meticillin-resistant Staphylococcus aureus ST22 widespread in communities of the Gaza Strip, 2009","volume":"23","author":"Chang","year":"2018","journal-title":"Eurosurveillance"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1809","DOI":"10.1017\/S0950268812000593","article-title":"An outbreak of post-partum breast abscesses in Mumbai, India caused by ST22-MRSA-IV: Genetic characteristics and epidemiological implications","volume":"140","author":"Manoharan","year":"2012","journal-title":"Epidemiol. Infect."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"250","DOI":"10.3201\/eid1502.080010","article-title":"Methicillin-susceptible Staphylococcus aureus in skin and soft tissue infections, Northern Italy","volume":"15","author":"Tinelli","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2069","DOI":"10.1093\/cid\/cix539","article-title":"Investigation of a Cluster of Sequence Type 22 Methicillin-Resistant\u00a0Staphylococcus aureus Transmission in a Community Setting","volume":"65","author":"Toleman","year":"2017","journal-title":"Clin. Infect. Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1541","DOI":"10.1007\/s10096-016-2695-8","article-title":"Molecular characterization of\u00a0Staphylococcus aureus isolates causing skin and soft tissue infections in patients from Malakand, Pakistan","volume":"35","author":"Madzgalla","year":"2016","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1099\/jmm.0.014910-0","article-title":"Epidemiological typing of meticillin-resistant\u00a0Staphylococcus aureus isolates from Pakistan and India","volume":"59","author":"Shabir","year":"2010","journal-title":"J. Med. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1099\/jmm.0.022707-0","article-title":"Prevalent genotypes of meticillin-resistant Staphylococcus aureus: Report from Pakistan","volume":"60","author":"Zafar","year":"2011","journal-title":"J. Med. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1016\/j.meegid.2013.04.026","article-title":"Genetics Evolution. Population genetics and the evolution of virulence in Staphylococcus aureus","volume":"21","author":"Chua","year":"2014","journal-title":"Infect. Genet. Evol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3526","DOI":"10.1128\/JCM.01168-12","article-title":"Comparative Whole-Genome Mapping to Determine\u00a0Staphylococcus aureus Genome Size, Virulence Motifs, and Clonality","volume":"50","author":"Shukla","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1719","DOI":"10.2147\/IDR.S202906","article-title":"Molecular typing revealed the emergence of pvl-positive sequence type 22 methicillin-susceptible\u00a0Staphylococcus aureus in Urumqi, Northwestern China","volume":"12","author":"Yuan","year":"2019","journal-title":"Infect. Drug Resist."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.ijfoodmicro.2003.10.002","article-title":"Use of novel PCR primers specific to the genes of staphylococcal enterotoxin G, H, I for the survey of\u00a0Staphylococcus aureus strains isolated from food-poisoning cases and food samples in Taiwan","volume":"92","author":"Chen","year":"2004","journal-title":"Int. J. Food Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1310","DOI":"10.1128\/JB.188.4.1310-1315.2006","article-title":"The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of\u00a0Staphylococcus aureus are located on \u03b2-hemolysin-converting bacteriophages","volume":"188","author":"Rooijakkers","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_36","first-page":"179","article-title":"Bacteriophage Therapy: An alternative for the treatment of\u00a0Staphylococcus aureus infections in animals and animal models","volume":"10","year":"2017","journal-title":"Front. Staphylococcus Aureus"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"14838","DOI":"10.1038\/s41598-020-71653-z","article-title":"The type VII secretion system protects\u00a0Staphylococcus aureus against antimicrobial host fatty acids","volume":"10","author":"Tchoupa","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1169","DOI":"10.1073\/pnas.0405620102","article-title":"EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of\u00a0Staphylococcus aureus infections","volume":"102","author":"Burts","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12864-019-5929-1","article-title":"Screening of genes encoding adhesion factors and biofilm production in methicillin resistant strains of\u00a0Staphylococcus aureus isolated from Palestinian patients","volume":"20","author":"Azmi","year":"2019","journal-title":"BMC Genom."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"98","DOI":"10.4014\/jmb.1410.10005","article-title":"Comparative genomic analysis of Staphylococcus aureus FORC_001 and S. aureus MRSA252 reveals the characteristics of antibiotic resistance and virulence factors for human infection","volume":"25","author":"Lim","year":"2015","journal-title":"J. Microbiol. Biotechnol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2723","DOI":"10.1016\/j.jksus.2020.06.007","article-title":"Antibiogram and plasmid profiling of beta-lactamase producing multi drug resistant Staphylococcus aureus isolated from poultry litter","volume":"32","author":"Pugazhendhi","year":"2020","journal-title":"J. King Saud Univ. -Sci."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Vogel, V., Falquet, L., Calderon-Copete, S.P., Basset, P., and Blanc, D.S. (2012). Short term evolution of a highly transmissible methicillin-resistant\u00a0Staphylococcus aureus clone (ST228) in a tertiary care hospital. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0038969"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"E3801","DOI":"10.1073\/pnas.1523199113","article-title":"Comparative genome-scale modelling of\u00a0Staphylococcus aureus strains identifies strain-specific metabolic capabilities linked to pathogenicity","volume":"113","author":"Bosi","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1186\/s12879-020-4866-6","article-title":"A comparative genomic analysis between methicillin-resistant\u00a0Staphylococcus aureus strains of hospital acquired and community infections in Yunnan province of China","volume":"20","author":"Liao","year":"2020","journal-title":"BMC Infect. Dis."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"9041636","DOI":"10.1155\/2016\/9041636","article-title":"Biochemical and molecular analysis of\u00a0Staphylococcus aureus clinical isolates from hospitalized patients","volume":"2016","author":"Karmakar","year":"2016","journal-title":"Can. J. Infect. Dis. Med. Microbiol."},{"key":"ref_46","first-page":"29","article-title":"Performance standards for antimicrobial susceptibility testing: Twenty-fifth informational supplement","volume":"35","author":"Patel","year":"2015","journal-title":"Clin. Lab. Stand. Inst."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"6614","DOI":"10.1093\/nar\/gkw569","article-title":"NCBI prokaryotic genome annotation pipeline","volume":"44","author":"Tatusova","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1394","DOI":"10.1101\/gr.2289704","article-title":"Mauve: Multiple alignment of conserved genomic sequence with rearrangements","volume":"14","author":"Darling","year":"2004","journal-title":"Genome Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1186\/1471-2164-13-202","article-title":"Comparing thousands of circular genomes using the CGView Comparison Tool","volume":"13","author":"Grant","year":"2012","journal-title":"BMC Genom."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e00612-17","DOI":"10.1128\/mSphere.00612-17","article-title":"SCCmecFinder, a Web-Based Tool for Typing of Staphylococcal Cassette Chromosome mec in Staphylococcus aureus Using Whole-Genome Sequence Data","volume":"3","author":"Kaya","year":"2018","journal-title":"mSphere"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1128\/JCM.06094-11","article-title":"Multilocus Sequence Typing of Total-Genome-Sequenced Bacteria","volume":"50","author":"Larsen","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"4305","DOI":"10.1128\/JCM.01979-14","article-title":"Comparing Whole-Genome Sequencing with Sanger Sequencing for spa Typing of Methicillin-Resistant Staphylococcus aureus","volume":"52","author":"Bartels","year":"2014","journal-title":"J. Clin. Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"3491","DOI":"10.1093\/jac\/dkaa345","article-title":"ResFinder 4.0 for predictions of phenotypes from genotypes","volume":"75","author":"Bortolaia","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"D325","DOI":"10.1093\/nar\/gki008","article-title":"VFDB: A reference database for bacterial virulence factors","volume":"33","author":"Chen","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"3895","DOI":"10.1128\/AAC.02412-14","article-title":"In Silico Detection and Typing of Plasmids using PlasmidFinder and Plasmid Multilocus Sequence Typing","volume":"58","author":"Carattoli","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"D195","DOI":"10.1093\/nar\/gky1050","article-title":"PLSDB: A resource of complete bacterial plasmids","volume":"47","author":"Galata","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"W16","DOI":"10.1093\/nar\/gkw387","article-title":"PHASTER: A better, faster version of the PHAST phage search tool","volume":"44","author":"Arndt","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Price, M.N., Dehal, P.S., and Arkin, A.P. (2010). FastTree 2-Approximately Maximum-Likelihood Trees for Large Alignments. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009490"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Kaas, R.S., Leekitcharoenphon, P., Aarestrup, F.M., and Lund, O. (2014). Solving the Problem of Comparing Whole Bacterial Genomes across Different Sequencing Platforms. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0104984"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"W256","DOI":"10.1093\/nar\/gkz239","article-title":"Interactive Tree of Life (iTOL) v4: Recent updates and new developments","volume":"47","author":"Letunic","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: Rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1186\/s12859-019-2713-9","article-title":"PanRV: Pangenome-reverse vaccinology approach for identifications of potential vaccine candidates in microbial pangenome","volume":"20","author":"Naz","year":"2019","journal-title":"BMC Bioinform."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"3691","DOI":"10.1093\/bioinformatics\/btv421","article-title":"Roary: Rapid large-scale prokaryote pan genome analysis","volume":"31","author":"Page","year":"2015","journal-title":"Bioinformatics"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"D261","DOI":"10.1093\/nar\/gku1223","article-title":"Expanded microbial genome coverage and improved protein family annotation in the COG database","volume":"43","author":"Galperin","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1093\/nar\/28.1.33","article-title":"The COG database: A tool for genome-scale analysis of protein functions and evolution","volume":"28","author":"Tatusov","year":"2000","journal-title":"Nucleic Acids Res."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/11\/4\/496\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:50:13Z","timestamp":1760136613000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/11\/4\/496"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,8]]},"references-count":67,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2022,4]]}},"alternative-id":["antibiotics11040496"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics11040496","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,8]]}}}