{"id":"https://openalex.org/W7224134808","doi":"https://doi.org/10.1186/s12864-026-13492-2","title":"Population-scale analysis of prophages and defense systems reveals distinct evolutionary routes for virulence and antimicrobial resistance in Staphylococcus aureus","display_name":"Population-scale analysis of prophages and defense systems reveals distinct evolutionary routes for virulence and antimicrobial resistance in Staphylococcus aureus","publication_year":2026,"publication_date":"2026-10-28","ids":{"openalex":"https://openalex.org/W7224134808","doi":"https://doi.org/10.1186/s12864-026-13492-2"},"language":"en","primary_location":{"id":"doi:10.1186/s12864-026-13492-2","doi":"https://doi.org/10.1186/s12864-026-13492-2","is_oa":true,"landing_page_url":"https://doi.org/10.1186/s12864-026-13492-2","pdf_url":null,"source":{"id":"https://openalex.org/S28614077","display_name":"BMC Genomics","issn_l":"1471-2164","issn":["1471-2164"],"is_oa":true,"is_in_doaj":true,"is_core":true,"listed_in":["anvur-scientific","cwts-core","doaj","dongbi-c","doyens","jufo-1","ki-jl-1","medline","norway-1","oarl","poland-140","russia-white-list-1","vabb-shw"],"host_organization":"https://openalex.org/P4310320256","host_organization_name":"BioMed Central","host_organization_lineage":["https://openalex.org/P4310320256","https://openalex.org/P4310319965"],"host_organization_lineage_names":["BioMed Central","Springer Nature"],"type":"journal"},"license":"cc-by-nc-nd","license_id":"https://openalex.org/licenses/cc-by-nc-nd","version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"BMC Genomics","raw_type":"journal-article"},"volume":null,"type":"article","indexed_in":["crossref","doaj"],"open_access":{"is_oa":true,"oa_status":"gold","oa_url":"https://doi.org/10.1186/s12864-026-13492-2","any_repository_has_fulltext":false},"authorships":[{"author_position":"first","author":{"id":"https://openalex.org/A5100644466","display_name":"Zhiqian Wang","orcid":"https://orcid.org/0000-0002-8303-3558","observed_orcids":["https://orcid.org/0000-0002-8303-3558"]},"institutions":[{"id":"https://openalex.org/I4210111013","display_name":"Nanjing Drum Tower Hospital","ror":"https://ror.org/026axqv54","country_code":"CN","type":"healthcare","lineage":["https://openalex.org/I4210111013"]}],"countries":["CN"],"is_corresponding":false,"raw_author_name":"Zhiqian Wang","raw_affiliation_strings":["Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China","institution_ids":["https://openalex.org/I4210111013"]}]},{"author_position":"middle","author":{"id":"https://openalex.org/A5160016395","display_name":"Guanghao Song","orcid":null,"observed_orcids":[]},"institutions":[{"id":"https://openalex.org/I4210111013","display_name":"Nanjing Drum Tower Hospital","ror":"https://ror.org/026axqv54","country_code":"CN","type":"healthcare","lineage":["https://openalex.org/I4210111013"]}],"countries":["CN"],"is_corresponding":false,"raw_author_name":"Guanghao Song","raw_affiliation_strings":["Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China","institution_ids":["https://openalex.org/I4210111013"]}]},{"author_position":"middle","author":{"id":"https://openalex.org/A5059048468","display_name":"Xiaohan Hu","orcid":null,"observed_orcids":[]},"institutions":[{"id":"https://openalex.org/I4210111013","display_name":"Nanjing Drum Tower Hospital","ror":"https://ror.org/026axqv54","country_code":"CN","type":"healthcare","lineage":["https://openalex.org/I4210111013"]}],"countries":["CN"],"is_corresponding":false,"raw_author_name":"Xiaohan Hu","raw_affiliation_strings":["Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China","institution_ids":["https://openalex.org/I4210111013"]}]},{"author_position":"middle","author":{"id":"https://openalex.org/A5101854161","display_name":"Shuo Gao","orcid":"https://orcid.org/0000-0002-8300-7675","observed_orcids":["https://orcid.org/0000-0002-8300-7675"]},"institutions":[{"id":"https://openalex.org/I4210111013","display_name":"Nanjing Drum Tower Hospital","ror":"https://ror.org/026axqv54","country_code":"CN","type":"healthcare","lineage":["https://openalex.org/I4210111013"]}],"countries":["CN"],"is_corresponding":false,"raw_author_name":"Shuo Gao","raw_affiliation_strings":["Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China","institution_ids":["https://openalex.org/I4210111013"]}]},{"author_position":"middle","author":{"id":"https://openalex.org/A5160050707","display_name":"Yan Zhang","orcid":null,"observed_orcids":[]},"institutions":[{"id":"https://openalex.org/I4210111013","display_name":"Nanjing Drum Tower Hospital","ror":"https://ror.org/026axqv54","country_code":"CN","type":"healthcare","lineage":["https://openalex.org/I4210111013"]}],"countries":["CN"],"is_corresponding":false,"raw_author_name":"Yan Zhang","raw_affiliation_strings":["Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China","institution_ids":["https://openalex.org/I4210111013"]}]},{"author_position":"middle","author":{"id":"https://openalex.org/A5112109350","display_name":"Xiaoli Cao","orcid":"https://orcid.org/0009-0008-0236-9094","observed_orcids":["https://orcid.org/0009-0008-0236-9094"]},"institutions":[{"id":"https://openalex.org/I4210111013","display_name":"Nanjing Drum Tower Hospital","ror":"https://ror.org/026axqv54","country_code":"CN","type":"healthcare","lineage":["https://openalex.org/I4210111013"]}],"countries":["CN"],"is_corresponding":true,"raw_author_name":"Xiaoli Cao","raw_affiliation_strings":["Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China","institution_ids":["https://openalex.org/I4210111013"]}]},{"author_position":"last","author":{"id":"https://openalex.org/A5077561975","display_name":"Zhou Wanqing","orcid":null,"observed_orcids":[]},"institutions":[{"id":"https://openalex.org/I4210111013","display_name":"Nanjing Drum Tower Hospital","ror":"https://ror.org/026axqv54","country_code":"CN","type":"healthcare","lineage":["https://openalex.org/I4210111013"]}],"countries":["CN"],"is_corresponding":true,"raw_author_name":"Wanqing Zhou","raw_affiliation_strings":["Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China"],"raw_orcid":null,"affiliations":[{"raw_affiliation_string":"Department of Clinical Laboratory, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing, Jiangsu, China","institution_ids":["https://openalex.org/I4210111013"]}]}],"institutions":[],"countries_distinct_count":1,"institutions_distinct_count":1,"corresponding_author_ids":["https://openalex.org/A5077561975","https://openalex.org/A5112109350"],"corresponding_institution_ids":["https://openalex.org/I4210111013"],"apc_list":{"value":3090,"currency":"USD","value_usd":3090},"apc_paid":{"value":3090,"currency":"USD","value_usd":3090},"fwci":0.0,"has_fulltext":false,"cited_by_count":0,"citation_normalized_percentile":{"value":0.84063232,"is_in_top_1_percent":false,"is_in_top_10_percent":false},"cited_by_percentile_year":null,"biblio":{"volume":null,"issue":null,"first_page":null,"last_page":null},"is_retracted":false,"is_paratext":false,"is_xpac":false,"primary_topic":{"id":"https://openalex.org/T10195","display_name":"Antimicrobial Resistance in Staphylococcus","score":0.9253000020980835,"subfield":{"id":"https://openalex.org/subfields/2725","display_name":"Infectious Diseases"},"field":{"id":"https://openalex.org/fields/27","display_name":"Medicine"},"domain":{"id":"https://openalex.org/domains/4","display_name":"Health Sciences"}},"topics":[{"id":"https://openalex.org/T10195","display_name":"Antimicrobial Resistance in Staphylococcus","score":0.9253000020980835,"subfield":{"id":"https://openalex.org/subfields/2725","display_name":"Infectious Diseases"},"field":{"id":"https://openalex.org/fields/27","display_name":"Medicine"},"domain":{"id":"https://openalex.org/domains/4","display_name":"Health Sciences"}},{"id":"https://openalex.org/T11048","display_name":"Bacteriophages and microbial interactions","score":0.06930000334978104,"subfield":{"id":"https://openalex.org/subfields/2406","display_name":"Virology"},"field":{"id":"https://openalex.org/fields/24","display_name":"Immunology and Microbiology"},"domain":{"id":"https://openalex.org/domains/1","display_name":"Life Sciences"}},{"id":"https://openalex.org/T11764","display_name":"Evolution and Genetic Dynamics","score":0.0008999999845400453,"subfield":{"id":"https://openalex.org/subfields/1311","display_name":"Genetics"},"field":{"id":"https://openalex.org/fields/13","display_name":"Biochemistry, Genetics and Molecular Biology"},"domain":{"id":"https://openalex.org/domains/1","display_name":"Life Sciences"}}],"keywords":[{"id":"https://openalex.org/keywords/staphylococcus-aureus","display_name":"Staphylococcus aureus","score":0.9150000214576721},{"id":"https://openalex.org/keywords/prophages","display_name":"prophages","score":0.9359999895095825},{"id":"https://openalex.org/keywords/virulence","display_name":"virulence","score":0.6510000228881836},{"id":"https://openalex.org/keywords/antimicrobial-resistance","display_name":"antimicrobial resistance","score":0.9959999918937683},{"id":"https://openalex.org/keywords/population-genomics","display_name":"population genomics","score":0.5849999785423279},{"id":"https://openalex.org/keywords/evolutionary-pathways","display_name":"evolutionary pathways","score":0.4059999883174896}],"concepts":[{"id":"https://openalex.org/C73445445","wikidata":"https://www.wikidata.org/wiki/Q1712327","display_name":"Prophage","level":5,"score":0.923799991607666},{"id":"https://openalex.org/C86803240","wikidata":"https://www.wikidata.org/wiki/Q420","display_name":"Biology","level":0,"score":0.8985999822616577},{"id":"https://openalex.org/C60987743","wikidata":"https://www.wikidata.org/wiki/Q1460232","display_name":"Virulence","level":3,"score":0.8201000094413757},{"id":"https://openalex.org/C2779489039","wikidata":"https://www.wikidata.org/wiki/Q188121","display_name":"Staphylococcus aureus","level":3,"score":0.7206000089645386},{"id":"https://openalex.org/C89423630","wikidata":"https://www.wikidata.org/wiki/Q7193","display_name":"Microbiology","level":1,"score":0.6741999983787537},{"id":"https://openalex.org/C94665300","wikidata":"https://www.wikidata.org/wiki/Q63391344","display_name":"Antibiotic resistance","level":3,"score":0.5281999707221985},{"id":"https://openalex.org/C54355233","wikidata":"https://www.wikidata.org/wiki/Q7162","display_name":"Genetics","level":1,"score":0.5202999711036682},{"id":"https://openalex.org/C4937899","wikidata":"https://www.wikidata.org/wiki/Q68541106","display_name":"Antimicrobial","level":2,"score":0.3968999981880188},{"id":"https://openalex.org/C523546767","wikidata":"https://www.wikidata.org/wiki/Q10876","display_name":"Bacteria","level":2,"score":0.35420000553131104},{"id":"https://openalex.org/C114851261","wikidata":"https://www.wikidata.org/wiki/Q12147416","display_name":"Drug resistance","level":2,"score":0.34850001335144043},{"id":"https://openalex.org/C180223184","wikidata":"https://www.wikidata.org/wiki/Q4839986","display_name":"Bacterial genetics","level":4,"score":0.3361000120639801},{"id":"https://openalex.org/C159047783","wikidata":"https://www.wikidata.org/wiki/Q7215","display_name":"Virology","level":1,"score":0.3319000005722046},{"id":"https://openalex.org/C2777334864","wikidata":"https://www.wikidata.org/wiki/Q34879","display_name":"Staphylococcal infections","level":4,"score":0.3248000144958496},{"id":"https://openalex.org/C95371953","wikidata":"https://www.wikidata.org/wiki/Q591745","display_name":"DNA microarray","level":4,"score":0.32269999384880066},{"id":"https://openalex.org/C2776460866","wikidata":"https://www.wikidata.org/wiki/Q170065","display_name":"Pathogen","level":2,"score":0.3215999901294708},{"id":"https://openalex.org/C64502627","wikidata":"https://www.wikidata.org/wiki/Q170065","display_name":"Pathogenicity","level":2,"score":0.32100000977516174},{"id":"https://openalex.org/C141231307","wikidata":"https://www.wikidata.org/wiki/Q7020","display_name":"Genome","level":3,"score":0.3165999948978424},{"id":"https://openalex.org/C57473165","wikidata":"https://www.wikidata.org/wiki/Q7315604","display_name":"Resistance (ecology)","level":2,"score":0.305400013923645},{"id":"https://openalex.org/C2993175405","wikidata":"https://www.wikidata.org/wiki/Q8054","display_name":"Bacterial protein","level":3,"score":0.28439998626708984},{"id":"https://openalex.org/C90132467","wikidata":"https://www.wikidata.org/wiki/Q171184","display_name":"Phylogenetics","level":3,"score":0.2687999904155731},{"id":"https://openalex.org/C2779288629","wikidata":"https://www.wikidata.org/wiki/Q199695","display_name":"Staphylococcus","level":4,"score":0.2651999890804291}],"mesh":[],"locations_count":1,"locations":[{"id":"doi:10.1186/s12864-026-13492-2","doi":"https://doi.org/10.1186/s12864-026-13492-2","is_oa":true,"landing_page_url":"https://doi.org/10.1186/s12864-026-13492-2","pdf_url":null,"source":{"id":"https://openalex.org/S28614077","display_name":"BMC Genomics","issn_l":"1471-2164","issn":["1471-2164"],"is_oa":true,"is_in_doaj":true,"is_core":true,"listed_in":["anvur-scientific","cwts-core","doaj","dongbi-c","doyens","jufo-1","ki-jl-1","medline","norway-1","oarl","poland-140","russia-white-list-1","vabb-shw"],"host_organization":"https://openalex.org/P4310320256","host_organization_name":"BioMed Central","host_organization_lineage":["https://openalex.org/P4310320256","https://openalex.org/P4310319965"],"host_organization_lineage_names":["BioMed Central","Springer Nature"],"type":"journal"},"license":"cc-by-nc-nd","license_id":"https://openalex.org/licenses/cc-by-nc-nd","version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"BMC Genomics","raw_type":"journal-article"}],"best_oa_location":{"id":"doi:10.1186/s12864-026-13492-2","doi":"https://doi.org/10.1186/s12864-026-13492-2","is_oa":true,"landing_page_url":"https://doi.org/10.1186/s12864-026-13492-2","pdf_url":null,"source":{"id":"https://openalex.org/S28614077","display_name":"BMC Genomics","issn_l":"1471-2164","issn":["1471-2164"],"is_oa":true,"is_in_doaj":true,"is_core":true,"listed_in":["anvur-scientific","cwts-core","doaj","dongbi-c","doyens","jufo-1","ki-jl-1","medline","norway-1","oarl","poland-140","russia-white-list-1","vabb-shw"],"host_organization":"https://openalex.org/P4310320256","host_organization_name":"BioMed Central","host_organization_lineage":["https://openalex.org/P4310320256","https://openalex.org/P4310319965"],"host_organization_lineage_names":["BioMed Central","Springer Nature"],"type":"journal"},"license":"cc-by-nc-nd","license_id":"https://openalex.org/licenses/cc-by-nc-nd","version":"publishedVersion","is_accepted":true,"is_published":true,"raw_source_name":"BMC Genomics","raw_type":"journal-article"},"sustainable_development_goals":[{"score":0.8048999905586243,"display_name":"Good health and well-being","id":"https://metadata.un.org/sdg/3"}],"study_designs":[],"awards":[],"funders":[],"has_content":{"pdf":false,"grobid_xml":false},"content_urls":null,"referenced_works_count":0,"referenced_works":[],"related_works":["https://openalex.org/W4380992975","https://openalex.org/W7099706515","https://openalex.org/W2809797843","https://openalex.org/W7118653824","https://openalex.org/W53104691","https://openalex.org/W4413165912","https://openalex.org/W7128729180","https://openalex.org/W7143790965","https://openalex.org/W2291779711","https://openalex.org/W4309512036"],"abstract_inverted_index":{"Staphylococcus":[0],"aureus":[1,37,309],"possesses":[2],"a":[3,146],"highly":[4],"dynamic":[5],"genome":[6],"shaped":[7],"by":[8,245],"both":[9],"mobile":[10],"genetic":[11],"elements":[12],"and":[13,25,50,59,67,82,101,133,205,287,304,323],"bacterial":[14,246],"defense":[15,23,42,111,126,157,168,301],"systems.":[16,169],"However,":[17,238],"the":[18,122,154,272,297,313],"population-scale":[19,294],"relationships":[20,298],"among":[21,299],"prophages,":[22,41,300],"systems,":[24,43,45,135,302],"functional":[26,277,288,322],"genes":[27,188,198,217,227],"remain":[28],"poorly":[29],"understood.":[30],"We":[31],"analyzed":[32],"1678":[33],"high-quality":[34],"complete":[35],"S.":[36,308],"genomes":[38],"to":[39,221],"identify":[40],"anti-defense":[44,134],"virulence":[46],"factor":[47],"(VF)":[48],"genes,":[49,180],"antimicrobial":[51,305],"resistance":[52,306],"(AMR)":[53],"genes.":[54,186,278,289],"Their":[55],"distribution,":[56],"co-occurrence":[57],"patterns,":[58],"associations":[60,191,241,284],"were":[61,75,116,140,199,218,228,251],"systematically":[62],"evaluated":[63],"using":[64],"comparative":[65],"genomic":[66,273],"statistical":[68],"approaches.":[69],"A":[70],"total":[71],"of":[72,85,156,175,268,275,319],"5249":[73],"prophages":[74,96,177,204,250,286],"predicted,":[76],"including":[77],"3439":[78],"classified":[79],"as":[80],"intact,":[81],"95.2%":[83],"(1598/1678)":[84],"strains":[86],"carried":[87,178],"at":[88],"least":[89],"one":[90],"predicted":[91],"intact":[92,95,176],"prophage.":[93],"These":[94],"comprised":[97],"76":[98],"distinct":[99,266],"types":[100],"exhibited":[102,206,281],"marked":[103],"sequence":[104],"type":[105],"(ST)-associated":[106],"distributions.":[107],"In":[108],"parallel,":[109],"45":[110],"systems":[112,120,127,158,280],"comprising":[113],"14,137":[114],"loci":[115],"identified,":[117],"with":[118,138,153,192,230,256,261,285],"restriction\u2013modification":[119],"being":[121],"most":[123,225],"abundant.":[124],"Multiple":[125],"frequently":[128,201,219,254],"co-occurred":[129],"within":[130],"individual":[131],"genomes,":[132],"predominantly":[136],"associated":[137,229,255],"anti-CRISPR,":[139],"also":[141],"detected.":[142],"Intact-prophage":[143],"abundance":[144],"showed":[145,189],"weak":[147],"but":[148],"statistically":[149],"significant":[150],"positive":[151],"correlation":[152],"number":[155],"(Spearman\u2019s":[159],"\u03c1":[160],"=":[161],"0.25),":[162],"which":[163],"persisted":[164],"after":[165],"excluding":[166],"prophage-encoded":[167],"Functional":[170],"annotation":[171],"revealed":[172,214],"that":[173,215],"56.3%":[174],"VF":[179,187,216,257],"whereas":[181,196,224],"only":[182],"4.3%":[183],"harbored":[184],"AMR":[185,197,226,262],"frequent":[190],"specific":[193],"prophage":[194,222,236,269],"types,":[195],"less":[200],"detected":[202],"in":[203,271,307],"more":[207,253],"restricted":[208],"association":[209],"patterns.":[210],"Network":[211],"analysis":[212],"further":[213,316],"linked":[220],"nodes,":[223],"defense-system":[231],"nodes":[232],"without":[233],"an":[234],"intervening":[235],"node.":[237],"some":[239],"observed":[240],"may":[242],"be":[243],"influenced":[244],"lineage":[247],"structure.":[248],"Intact":[249],"substantially":[252],"gene":[258,263],"carriage":[259],"than":[260],"carriage,":[264],"suggesting":[265],"patterns":[267],"involvement":[270],"distribution":[274],"these":[276,291],"Defense":[279],"heterogeneous,":[282],"system-specific":[283],"Together,":[290],"findings":[292],"provide":[293],"insights":[295],"into":[296],"virulence,":[303],",":[310],"while":[311],"highlighting":[312],"need":[314],"for":[315],"experimental":[317],"validation":[318],"their":[320],"potential":[321],"evolutionary":[324],"implications.":[325]},"counts_by_year":[],"updated_date":"2026-10-31T12:09:11.096373","created_date":"2026-10-29T00:00:00"}