{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T23:00:46Z","timestamp":1791327646023,"version":"4.3.1"},"reference-count":44,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2023,6,6]],"date-time":"2023-06-06T00:00:00Z","timestamp":1686009600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Australian Centre for Genomic Epidemiological Microbiology","award":["1.5.8"],"award-info":[{"award-number":["1.5.8"]}]},{"name":"Poultry Cooperative Research Centre","award":["1.5.8"],"award-info":[{"award-number":["1.5.8"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Bacterial chondronecrosis with osteomyelitis (BCO) impacts animal welfare and productivity in the poultry industry worldwide, yet it has an understudied pathogenesis. While Avian Pathogenic Escherichia coli (APEC) are known to be one of the main causes, there is a lack of whole genome sequence data, with only a few BCO-associated APEC (APECBCO) genomes available in public databases. In this study, we conducted an analysis of 205 APECBCO genome sequences to generate new baseline phylogenomic knowledge regarding the diversity of E. coli sequence types and the presence of virulence associated genes (VAGs). Our findings revealed the following: (i) APECBCO are phylogenetically and genotypically similar to APEC that cause colibacillosis (APECcolibac), with globally disseminated APEC sequence types ST117, ST57, ST69, and ST95 being predominate; (ii) APECBCO are frequent carriers of ColV-like plasmids that carry a similar set of VAGs as those found in APECcolibac. Additionally, we performed genomic comparisons, including a genome-wide association study, with a complementary collection of geotemporally-matched genomes of APEC from multiple cases of colibacillosis (APECcolibac). Our genome-wide association study found no evidence of novel virulence loci unique to APECBCO. Overall, our data indicate that APECBCO and APECcolibac are not distinct subpopulations of APEC. Our publication of these genomes substantially increases the available collection of APECBCO genomes and provides insights for the management and treatment strategies of lameness in poultry.<\/jats:p>","DOI":"10.3390\/microorganisms11061513","type":"journal-article","created":{"date-parts":[[2023,6,7]],"date-time":"2023-06-07T01:38:41Z","timestamp":1686101921000},"page":"1513","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Whole Genome Sequencing of Avian Pathogenic Escherichia coli Causing Bacterial Chondronecrosis and Osteomyelitis in Australian Poultry"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9333-7160","authenticated-orcid":false,"given":"Max L.","family":"Cummins","sequence":"first","affiliation":[{"name":"Australian Institute for Microbiology and Infection, University of Technology Sydney, Ultimo, NSW 2007, Australia"},{"name":"The Australian Centre for Genomic Epidemiological Microbiology, University of Technology Sydney, Ultimo, NSW 2007, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7535-8184","authenticated-orcid":false,"given":"Dmitriy","family":"Li","sequence":"additional","affiliation":[{"name":"Australian Institute for Microbiology and Infection, University of Technology Sydney, Ultimo, NSW 2007, Australia"},{"name":"The Australian Centre for Genomic Epidemiological Microbiology, University of Technology Sydney, Ultimo, NSW 2007, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aeman","family":"Ahmad","sequence":"additional","affiliation":[{"name":"Australian Institute for Microbiology and Infection, University of Technology Sydney, Ultimo, NSW 2007, Australia"},{"name":"The Australian Centre for Genomic Epidemiological Microbiology, University of Technology Sydney, Ultimo, NSW 2007, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1159-7394","authenticated-orcid":false,"given":"Rhys","family":"Bushell","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amir H.","family":"Noormohammadi","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dinidu S.","family":"Wijesurendra","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4432-8185","authenticated-orcid":false,"given":"Andrew","family":"Stent","sequence":"additional","affiliation":[{"name":"Gribbles Veterinary Pathology, Clayton, VIC 3168, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6778-1110","authenticated-orcid":false,"given":"Marc S.","family":"Marenda","sequence":"additional","affiliation":[{"name":"Faculty of Science, The University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9301-5372","authenticated-orcid":false,"given":"Steven P.","family":"Djordjevic","sequence":"additional","affiliation":[{"name":"Australian Institute for Microbiology and Infection, University of Technology Sydney, Ultimo, NSW 2007, Australia"},{"name":"The Australian Centre for Genomic Epidemiological Microbiology, University of Technology Sydney, Ultimo, NSW 2007, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,6,6]]},"reference":[{"key":"ref_1","unstructured":"Nolan, L.K., Barnes, H.J., Vaillancourt, J.-P., Abdul-Aziz, T., and Logue, C.M. (2013). Diseases of Poultry, John Wiley & Sons."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Maluta, R.P., Logue, C.M., Casas, M.R., Meng, T., Guastalli, E.A., Rojas, T.C., Montelli, A.C., Sadatsune, T., de Carvalho Ramos, M., and Nolan, L.K. (2014). Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0105016"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1089\/fpd.2014.1815","article-title":"Molecular characterization and clonal relationships among Escherichia coli strains isolated from broiler chickens with colisepticemia","volume":"12","author":"Barbieri","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_4","first-page":"299","article-title":"Avian pathogenic Escherichia coli (APEC)","volume":"30","author":"Fairbrother","year":"1999","journal-title":"Vet. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3389\/fvets.2014.00005","article-title":"Is the Concept of Avian Pathogenic Escherichia coli as a Single Pathotype Fundamentally Flawed?","volume":"1","author":"Collingwood","year":"2014","journal-title":"Front. Vet. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"325","DOI":"10.3382\/ps\/pev320","article-title":"Bacterial chondronecrosis with osteomyelitis and lameness in broilers: A review","volume":"95","author":"Wideman","year":"2016","journal-title":"Poult. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1080\/03079457.2017.1349872","article-title":"Pathological and microbiological investigations into cases of bacterial chondronecrosis and osteomyelitis in broiler poultry","volume":"46","author":"Wijesurendra","year":"2017","journal-title":"Avian Pathol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1080\/030794500750047243","article-title":"Bacterial chondronecrosis with osteomyelitis (\u2018femoral head necrosis\u2019) of broiler chickens: A review","volume":"29","author":"McNamee","year":"2000","journal-title":"Avian Pathol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"101457","DOI":"10.1016\/j.psj.2021.101457","article-title":"Impact of experimentally induced bacterial chondronecrosis with osteomyelitis (BCO) lameness on health, stress, and leg health parameters in broilers","volume":"100","author":"Weimer","year":"2021","journal-title":"Poult. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1089\/fpd.2011.0961","article-title":"Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from humans and poultry","volume":"9","author":"Johnson","year":"2012","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1051\/vetres:2004057","article-title":"Characterizing the APEC pathotype","volume":"36","author":"Giddings","year":"2005","journal-title":"Vet. Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1038\/s41467-021-20988-w","article-title":"Genome evolution and the emergence of pathogenicity in avian Escherichia coli","volume":"12","author":"Mageiros","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"6287","DOI":"10.1128\/IAI.00363-06","article-title":"Acquisition of avian pathogenic Escherichia coli plasmids by a commensal E. coli isolate enhances its abilities to kill chicken embryos, grow in human urine, and colonize the murine kidney","volume":"74","author":"Skyberg","year":"2006","journal-title":"Infect. Immun."},{"key":"ref_14","first-page":"e000250","article-title":"Whole genome sequence analysis of Australian avian pathogenic Escherichia coli that carry the class 1 integrase gene","volume":"5","author":"Cummins","year":"2019","journal-title":"Microb. Genom."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Poulsen, L.L., Kudirkiene, E., J\u00f8rgensen, S.L., Djordjevic, S.P., Cummins, M.L., Christensen, J.P., Christensen, H., Bisgaard, M., and Th\u00f8fner, I. (2020). Whole genome sequence comparison of avian pathogenic Escherichia coli from acute and chronic salpingitis of egg laying hens. BMC Vet. Res., 16.","DOI":"10.1186\/s12917-020-02369-5"},{"key":"ref_16","first-page":"e000143","article-title":"Porcine commensal Escherichia coli: A reservoir for class 1 integrons associated with IS26","volume":"3","author":"Reid","year":"2017","journal-title":"Microb. Genom."},{"key":"ref_17","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_18","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1101\/gr.186072.114","article-title":"CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes","volume":"25","author":"Parks","year":"2015","journal-title":"Genome Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2538","DOI":"10.1128\/JCM.00737-17","article-title":"Development of a web tool for Escherichia coli subtyping based on fimH alleles","volume":"55","author":"Roer","year":"2017","journal-title":"J. Clin. Microbiol."},{"key":"ref_20","first-page":"000728","article-title":"ECTyper: In silico Escherichia coli serotype and species prediction from raw and assembled whole-genome sequence data","volume":"7","author":"Bessonov","year":"2021","journal-title":"Microb. Genom."},{"key":"ref_21","first-page":"e000192","article-title":"ClermonTyping: An easy-to-use and accurate in silico method for Escherichia genus strain phylotyping","volume":"4","author":"Beghain","year":"2018","journal-title":"Microb. Genom."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e000143","DOI":"10.1099\/acmi.0.000143","article-title":"Easy phylotyping of Escherichia coli via the EzClermont web app and command-line tool","volume":"2","author":"Waters","year":"2020","journal-title":"Access Microbiol."},{"key":"ref_23","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_24","doi-asserted-by":"crossref","unstructured":"Zhou, Z., Alikhan, N.-F., Mohamed, K., Fan, Y., Agama Study Group, and Achtman, M. (2019). The user\u2019s guide to comparative genomics with EnteroBase, including case studies on transmissions of micro-clades of Salmonella, the phylogeny of ancient and modern Yersinia pestis genomes, and the core genomic diversity of all Escherichia. bioRxiv, 613554.","DOI":"10.1101\/613554"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"D32","DOI":"10.1093\/nar\/gkj014","article-title":"ISfinder: The reference centre for bacterial insertion sequences","volume":"34","author":"Siguier","year":"2006","journal-title":"Nucleic Acids Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1038\/s41467-022-35713-4","article-title":"An ISO-certified genomics workflow for identification and surveillance of antimicrobial resistance","volume":"14","author":"Sherry","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"12728","DOI":"10.1038\/s41598-021-91456-0","article-title":"AMRFinderPlus and the Reference Gene Catalog facilitate examination of the genomic links among antimicrobial resistance, stress response, and virulence","volume":"11","author":"Feldgarden","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_28","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_29","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1186\/s13059-020-02090-4","article-title":"Producing polished prokaryotic pangenomes with the Panaroo pipeline","volume":"21","author":"MacAlasdair","year":"2020","journal-title":"Genome Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2520","DOI":"10.1093\/bioinformatics\/bts480","article-title":"Snakemake\u2014A scalable bioinformatics workflow engine","volume":"28","author":"Rahmann","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1186\/s13059-016-1108-8","article-title":"Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary","volume":"17","author":"Brynildsrud","year":"2016","journal-title":"Genome Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_33","first-page":"1","article-title":"Package \u2018vegan\u2019","volume":"2","author":"Oksanen","year":"2013","journal-title":"Community Ecol. Package Version"},{"key":"ref_34","unstructured":"Venables, W.N., and Ripley, B.D. (2013). Modern Applied Statistics with S-PLUS, Springer Science & Business Media."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"e00470-18","DOI":"10.1128\/mBio.00470-18","article-title":"Escherichia coli ST131-H22 as a foodborne uropathogen","volume":"9","author":"Liu","year":"2018","journal-title":"mBio"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Page, A.J., Taylor, B., Delaney, A.J., Soares, J., Seemann, T., Keane, J.A., and Harris, S.R. (2016). SNP-sites: Rapid efficient extraction of SNPs from multi-FASTA alignments. bioRxiv, 038190.","DOI":"10.1101\/038190"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Harris, S.R. (2018). SKA: Split kmer analysis toolkit for bacterial genomic epidemiology. bioRxiv, 453142.","DOI":"10.1101\/453142"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1089\/fpd.2014.1860","article-title":"Multilocus sequence typing and virulence gene profiles associated with Escherichia coli from human and animal sources","volume":"12","author":"Manges","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1128\/JB.188.2.745-758.2006","article-title":"DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains","volume":"188","author":"Johnson","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3675","DOI":"10.1016\/j.psj.2020.03.064","article-title":"Role of LsrR in the regulation of antibiotic sensitivity in avian pathogenic Escherichia coli","volume":"99","author":"Yu","year":"2020","journal-title":"Poult. Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1128\/JB.188.1.305-316.2006","article-title":"Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022)","volume":"188","author":"Zuo","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1128\/jb.158.2.665-673.1984","article-title":"D-ribose metabolism in Escherichia coli K-12: Genetics, regulation, and transport","volume":"158","author":"Lopilato","year":"1984","journal-title":"J. Bacteriol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.ijfoodmicro.2005.06.023","article-title":"Detection of sul1, sul2 and sul3 in sulphonamide resistant Escherichia coli isolates obtained from healthy humans, pork and pigs in Denmark","volume":"106","author":"Hammerum","year":"2006","journal-title":"Int. J. Food Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/6\/1513\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:49:26Z","timestamp":1760125766000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/6\/1513"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,6]]},"references-count":44,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["microorganisms11061513"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms11061513","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,6]]}}}