{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T20:29:39Z","timestamp":1792096179598,"version":"4.4.0"},"reference-count":57,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,9,23]],"date-time":"2025-09-23T00:00:00Z","timestamp":1758585600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p><jats:italic>Glaesserella parasuis<\/jats:italic> is an important bacterial pathogen and the etiological agent of Gl\u00e4sser\u2019s disease, which causes substantial economic losses on swine farms worldwide. Although large scale genome studies have been carried out in the North hemisphere, few genomes from South America are available limiting our knowledge of the full genetic diversity of this bacteria. In this study, seventeen clinical <jats:italic>G. parasuis<\/jats:italic> isolates from diseased swine in Peru where whole genome sequenced and compared with publicly available genomes. We identified seven distinct sequence types and five serotypes being more prevalent: the emergent ST454 and novel ST726 and serotypes 7 and 12. Although most isolates did not carried any antimicrobial resistance gene (ARG) we identified a large cassette of \u223c50 kb carrying nine different ARGs (<jats:italic>aac(3)-IV, aph(3\u2032)-Ia, aph(3\u2032)-Ib, sul2, bla<\/jats:italic><jats:sub><jats:italic>ROB\u2013<\/jats:italic>1<\/jats:sub><jats:italic>tetB, lnuH, estT<\/jats:italic> and <jats:italic>floR<\/jats:italic>) including six tandem repeats of <jats:italic>estT<\/jats:italic> and <jats:italic>floR<\/jats:italic> genes. We also identified two coexisting small plasmids harboring <jats:italic>tetH, estT<\/jats:italic> and <jats:italic>bla<\/jats:italic><jats:sub><jats:italic>ROB\u2013<\/jats:italic>1<\/jats:sub> in two isolates. Most of the isolates (88.2%, 15\/17) harbored at least one group 1 <jats:italic>vtaA<\/jats:italic> virulence gene. The <jats:italic>G. parasuis<\/jats:italic> diversity was segregated in two clades (C1 and C2) by phylogenetic and gene content analysis. We identified several genes overrepresented in both clades, however three metabolic operons (<jats:italic>glnHMPQ, hisGDCBHAFI, thiDEM<\/jats:italic>) were almost exclusive of C2 strains suggesting that C1 strains are auxotrophs for histidine and thiamine important nutrient for bacterial survival which may impact in the adaptation of these strains to the host niche. Our results suggest a high diversity of <jats:italic>G. parasuis<\/jats:italic> strains circulating in Peru, the presence of mobile elements carrying multiple ARGs underscores the need for continuous surveillance of this pathogen within the Peruvian swine industry to identify potential vaccine candidates and formulate better control programs.<\/jats:p>","DOI":"10.3389\/fmicb.2025.1678153","type":"journal-article","created":{"date-parts":[[2025,9,23]],"date-time":"2025-09-23T05:31:25Z","timestamp":1758605485000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Genomic insights into diversity, antimicrobial resistance and virulence of Glaesserella parasuis from diseased swine in Peru"],"prefix":"10.3389","volume":"16","author":[{"given":"Luis","family":"Alvarez-Vega","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karolina S. M.","family":"De La Cruz-Monroy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arturo","family":"Garcia-Barraza","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dennis","family":"Carhuaricra","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jose L.","family":"Llaja-Bernedo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liseth L.","family":"Huamancha-Pulido","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alejandra","family":"Medina-Gonzales","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andre F.","family":"Sedano-Sanchez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,9,23]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"e01716-20","DOI":"10.1128\/AAC.01716-20","article-title":"ICEHpsaHPS7, a novel multiple drug resistance integrative conjugative element in Glaesserella parasuis.","volume":"65","author":"An","year":"2021","journal-title":"Antimicrob. Agents Chemother."},{"key":"B2","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1016\/J.VETMIC.2009.10.025","article-title":"Correlation between clinico-pathological outcome and typing of Haemophilus parasuis field strains.","volume":"142","author":"Aragon","year":"2010","journal-title":"Vet. Microbiol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"844","DOI":"10.1002\/9781119350927.ch54","article-title":"\u201cGl\u00e1sser\u2019s disease\u201d, in","author":"Aragon","year":"2019","journal-title":"Diseases of Swine"},{"key":"B4","doi-asserted-by":"publisher","first-page":"502","DOI":"10.1136\/VR.151.17.502","article-title":"Protection of vaccinated pigs against experimental infections with homologous and heterologous Hoemophilus parasuis.","volume":"151","author":"Bak","year":"2002","journal-title":"Vet. Rec."},{"key":"B5","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1128\/JCM.33.1.37-40.1995","article-title":"Auxotrophic variants of Pseudomonas aeruginosa are selected from prototrophic wild-type strains in respiratory infections in patients with cystic fibrosis.","volume":"33","author":"Barth","year":"1995","journal-title":"J. Clin. Microbiol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"5825","DOI":"10.1093\/MOLBEV\/MSAB293","article-title":"eggNOG-mapper v2: Functional annotation, orthology assignments, and domain prediction at the metagenomic scale.","volume":"38","author":"Cantalapiedra","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1186\/1297-9716-43-57","article-title":"VtaA8 and VtaA9 from Haemophilus parasuis delay phagocytosis by alveolar macrophages.","volume":"43","author":"Costa-Hurtado","year":"2012","journal-title":"Vet. Res."},{"key":"B8","doi-asserted-by":"publisher","first-page":"108595","DOI":"10.1016\/J.VETMIC.2020.108595","article-title":"Update on Gl\u00e4sser\u2019s disease: How to control the disease under restrictive use of antimicrobials.","volume":"242","author":"Costa-Hurtado","year":"2020","journal-title":"Vet. Microbiol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/S13567-019-0687-2\/FIGURES\/5","article-title":"Haemophilus parasuis VtaA2 is involved in adhesion to extracellular proteins.","volume":"50","author":"Costa-Hurtado","year":"2019","journal-title":"Vet. Res."},{"key":"B10","doi-asserted-by":"publisher","first-page":"2559","DOI":"10.1111\/EVO.12468","article-title":"less is more: Selective advantages can explain the prevalent loss of biosynthetic genes in bacteria.","volume":"68","author":"D\u2019Souza","year":"2014","journal-title":"Evolution"},{"key":"B11","doi-asserted-by":"publisher","first-page":"e6817","DOI":"10.7717\/PEERJ.6817","article-title":"Molecular serotyping of clinical strains of Haemophilus (Glaesserella) parasuis brings new insights regarding Gl\u00e4sser\u2019s disease outbreaks in Brazil.","volume":"7","author":"Esp\u00edndola","year":"2019","journal-title":"PeerJ"},{"key":"B12","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1023\/A:1006531526299\/METRICS","article-title":"Evolution of the structure and chromosomal distribution of histidine biosynthetic genes.","volume":"28","author":"Fani","year":"1998","journal-title":"Origins Life Evol. Biosphere"},{"key":"B13","doi-asserted-by":"publisher","first-page":"e00869-17","DOI":"10.1128\/AAC.00869-17","article-title":"Tandem amplification of the staphylococcal cassette chromosome mec element can drive high-level methicillin resistance in methicillin-resistant staphylococcus aureus.","volume":"61","author":"Gallagher","year":"2017","journal-title":"Antimicrob. Agents Chemother."},{"key":"B14","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1186\/S12917-017-1041-4","article-title":"A robust PCR for the differentiation of potential virulent strains of Haemophilus parasuis.","volume":"13","author":"Galofr\u00e9-Mil\u00e0","year":"2017","journal-title":"BMC Vet. Res."},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1007\/0-387-28022-7","author":"Garrity","year":"2005","journal-title":"Bergey\u2019s manual of systematic bacteriology"},{"key":"B16","doi-asserted-by":"publisher","first-page":"e00231-24","DOI":"10.1128\/MSPHERE.00231-24","article-title":"Genomic insight into the diversity of Glaesserella parasuis isolates from 19 countries.","volume":"9","author":"Gong","year":"2024","journal-title":"mSphere"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.1093\/BIOINFORMATICS\/BTT086","article-title":"QUAST: Quality assessment tool for genome assemblies.","volume":"29","author":"Gurevich","year":"2013","journal-title":"Bioinformatics"},{"key":"B18","doi-asserted-by":"publisher","first-page":"110509","DOI":"10.1016\/J.VETMIC.2025.110509","article-title":"Capsular immunity is necessary for protection against some but not all strains of Glaesserella parasuis.","volume":"305","author":"Hau","year":"2025","journal-title":"Vet. Microbiol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"3812","DOI":"10.1128\/JCM.01991-15","article-title":"Development of a multiplex PCR assay for rapid molecular serotyping of Haemophilus parasuis.","volume":"53","author":"Howell","year":"2015","journal-title":"J. Clin. Microbiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/S13059-024-03252-4\/FIGURES\/3","article-title":"NextDenovo: An efficient error correction and accurate assembly tool for noisy long reads.","volume":"25","author":"Hu","year":"2024","journal-title":"Genome Biol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"5114","DOI":"10.1038\/s41467-018-07641-9","article-title":"High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries.","volume":"9","author":"Jain","year":"2018","journal-title":"Nat. Commun."},{"key":"B22","doi-asserted-by":"publisher","first-page":"3249","DOI":"10.1128\/JCM.00688-17","article-title":"Development of serotype-specific PCR assays for typing of haemophilus parasuis isolates circulating in Southern China.","volume":"55","author":"Jia","year":"2017","journal-title":"J. Clin. Microbiol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"862","DOI":"10.1128\/JCM.30.4.862-865.1992","article-title":"Designation of 15 serovars of Haemophilus parasuis on the basis of immunodiffusion using heat-stable antigen extracts.","volume":"30","author":"Kielstein","year":"1992","journal-title":"J. Clin. Microbiol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"btae311","DOI":"10.1093\/BIOINFORMATICS\/BTAE311","article-title":"Parsnp 2.0: Scalable core-genome alignment for massive microbial datasets.","volume":"40","author":"Kille","year":"2024","journal-title":"Bioinformatics"},{"key":"B25","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1038\/s41587-019-0072-8","article-title":"Assembly of long, error-prone reads using repeat graphs.","volume":"37","author":"Kolmogorov","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"722","DOI":"10.1101\/GR.215087.116","article-title":"Canu: Scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation.","volume":"27","author":"Koren","year":"2017","journal-title":"Genome Res."},{"key":"B27","doi-asserted-by":"publisher","first-page":"2103","DOI":"10.1093\/BIOINFORMATICS\/BTW152","article-title":"Minimap and miniasm: Fast mapping and de novo assembly for noisy long sequences.","volume":"32","author":"Li","year":"2016","journal-title":"Bioinformatics"},{"key":"B28","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/S13567-021-00935-9\/TABLES\/8","article-title":"Molecular characterization of Glaesserella parasuis strains isolated from North America, Europe and Asia by serotyping PCR and LS-PCR.","volume":"52","author":"Macedo","year":"2021","journal-title":"Vet. Res."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/S13567-015-0263-3\/METRICS","article-title":"Haemophilus parasuis: Infection, immunity and enrofloxacin.","volume":"46","author":"Macedo","year":"2015","journal-title":"Vet. Res."},{"key":"B30","author":"Markey","year":"2013","journal-title":"Clinical veterinary microbiology"},{"key":"B31","doi-asserted-by":"publisher","first-page":"2117","DOI":"10.1099\/MIC.0.056994-0","article-title":"Distribution of genes involved in sialic acid utilization in strains of Haemophilus parasuis.","volume":"158","author":"Mart\u00ednez-Moliner","year":"2012","journal-title":"Microbiology"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1530","DOI":"10.1093\/MOLBEV\/MSAA015","article-title":"IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era.","volume":"37","author":"Minh","year":"2020","journal-title":"Mol. Biol. Evol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1186\/S12917-023-03698-X\/FIGURES\/4","article-title":"Molecular characterization of Glaesserella parasuis strains circulating in North American swine production systems.","volume":"19","author":"Mugabi","year":"2023","journal-title":"BMC Vet. Res."},{"key":"B34","doi-asserted-by":"publisher","first-page":"899","DOI":"10.1016\/J.VETMIC.2012.11.019","article-title":"A curated public database for multilocus sequence typing (MLST) and analysis of Haemophilus parasuis based on an optimized typing scheme.","volume":"162","author":"Mullins","year":"2013","journal-title":"Vet. Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.vetmic.2003.12.001","article-title":"Haemophilus parasuis: New trends on diagnosis, epidemiology and control.","volume":"99","author":"Oliveira","year":"2004","journal-title":"Vet. Microbiol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1051\/VETRES\/2009074","article-title":"Virulence-associated trimeric autotransporters of Haemophilus parasuis are antigenic proteins expressed in vivo.","volume":"41","author":"Olvera","year":"2010","journal-title":"Vet. Res."},{"key":"B37","doi-asserted-by":"publisher","first-page":"3970","DOI":"10.1038\/s41467-020-17735-y","article-title":"Efflux pump activity potentiates the evolution of antibiotic resistance across S. aureus isolates.","volume":"11","author":"Papkou","year":"2020","journal-title":"Nat. Commun."},{"key":"B38","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1038\/s44259-024-00052-5","article-title":"Antibiotic resistance mediated by gene amplifications.","volume":"2","author":"Pavan","year":"2024","journal-title":"npj Antimicrob Resist."},{"key":"B39","doi-asserted-by":"publisher","first-page":"576","DOI":"10.1128\/JB.00703-08\/SUPPL_FILE\/TABLE_S2.ZIP","article-title":"Trimeric autotransporters of haemophilus parasuis: Generation of an extensive passenger domain repertoire specific for pathogenic strains.","volume":"191","author":"Pina","year":"2009","journal-title":"J. Bacteriol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1186\/S13059-024-03233-7\/TABLES\/1","article-title":"Scoary2: Rapid association of phenotypic multi-omics data with microbial pan-genomes.","volume":"25","author":"Roder","year":"2024","journal-title":"Genome Biol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1016\/J.VETMIC.2008.11.008","article-title":"Identification of novel potential virulence-associated factors in Haemophilus parasuis.","volume":"136","author":"Sack","year":"2009","journal-title":"Vet. Microbiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"3399","DOI":"10.1128\/AAC.01522-08\/ASSET\/D68F657D-4A08-4ACC-8166-43199BFEA181\/ASSETS\/GRAPHIC\/ZAC0080983520003.JPEG","article-title":"Multiresistance in Pasteurella multocida is mediated by coexistence of small plasmids.","volume":"53","author":"San Millan","year":"2009","journal-title":"Antimicrob. Agents Chemother."},{"key":"B43","doi-asserted-by":"publisher","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":"B44","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.1093\/BIOINFORMATICS\/BTR039","article-title":"Easyfig: A genome comparison visualizer.","volume":"27","author":"Sullivan","year":"2011","journal-title":"Bioinformatics"},{"key":"B45","doi-asserted-by":"publisher","first-page":"1884","DOI":"10.3389\/FMICB.2020.01884","article-title":"Molecular characterization of a novel integrative conjugative element ICE Hpa1 in Haemophilus parasuis.","volume":"11","author":"Sun","year":"2020","journal-title":"Front. Microbiol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"106740","DOI":"10.1016\/J.IJANTIMICAG.2023.106740","article-title":"ICEGpa1804, a novel integrative and conjugative element carrying eight resistance genes, identified in Glaesserella parasuis.","volume":"61","author":"Sun","year":"2023","journal-title":"Int. J. Antimicrob. Agents"},{"key":"B47","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1128\/JCM.42.2.839-840.2004","article-title":"Development of a new serological test for serotyping Haemophilus parasuis isolates and determination of their prevalence in North America.","volume":"42","author":"Tadjine","year":"2004","journal-title":"J. Clin. Microbiol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/S13059-020-02090-4\/FIGURES\/7","article-title":"Producing polished prokaryotic pangenomes with the Panaroo pipeline.","volume":"21","author":"Tonkin-Hill","year":"2020","journal-title":"Genome Biol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"1323","DOI":"10.1111\/J.1365-2672.2009.04526.X","article-title":"Validation of a real-time PCR for Haemophilus parasuis.","volume":"108","author":"Turni","year":"2010","journal-title":"J. Appl. Microbiol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1111\/AVJ.12705","article-title":"Virulence-associated gene profiling, DNA fingerprinting and multilocus sequence typing of Haemophilus parasuis isolates in Australia.","volume":"96","author":"Turni","year":"2018","journal-title":"Aust. Vet. J."},{"key":"B51","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/J.VETMIC.2019.02.008","article-title":"Characterization of serotypes and virulence genes of Haemophilus parasuis isolates from Central Vietnam.","volume":"230","author":"Van","year":"2019","journal-title":"Vet. Microbiol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"e9293","DOI":"10.7717\/PEERJ.9293\/SUPP-64","article-title":"Whole-genome sequence analyses of Glaesserella parasuis isolates reveals extensive genomic variation and diverse antibiotic resistance determinants.","volume":"2020","author":"Wan","year":"2020","journal-title":"PeerJ"},{"key":"B53","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1016\/J.MEEGID.2016.07.015","article-title":"Multilocus sequence typing and virulence analysis of Haemophilus parasuis strains isolated in five provinces of China.","volume":"44","author":"Wang","year":"2016","journal-title":"Infect. Genet. Evol."},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.1101\/2025.05.12.653612","article-title":"Autocycler: Long-read consensus assembly for bacterial genomes.","author":"Wick","year":"2025","journal-title":"bioRxiv [Preprint]"},{"key":"B55","doi-asserted-by":"publisher","first-page":"1084491","DOI":"10.3389\/FVETS.2023.1084491\/BIBTEX","article-title":"Characterization of small plasmids carrying florfenicol resistance gene floR in Actinobacillus pleuropneumoniae and Pasteurella multocida isolates from swine in China.","volume":"10","author":"Yao","year":"2023","journal-title":"Front. Vet. Sci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"e96","DOI":"10.1002\/CPBI.96","article-title":"Using ggtree to visualize data on tree-like structures.","volume":"69","author":"Yu","year":"2020","journal-title":"Curr. Protoc. Bioinformatics"},{"key":"B57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/J.VETMIC.2013.07.027","article-title":"Update on the pathogenesis of Haemophilus parasuis infection and virulence factors.","volume":"168","author":"Zhang","year":"2014","journal-title":"Vet. Microbiol."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2025.1678153\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,9,23]],"date-time":"2025-09-23T05:31:26Z","timestamp":1758605486000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2025.1678153\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,9,23]]},"references-count":57,"alternative-id":["10.3389\/fmicb.2025.1678153"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2025.1678153","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,9,23]]},"article-number":"1678153"}}