{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,3]],"date-time":"2026-11-03T17:59:07Z","timestamp":1793728747402,"version":"4.6.1"},"reference-count":44,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,1,20]],"date-time":"2022-01-20T00:00:00Z","timestamp":1642636800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,1,20]],"date-time":"2022-01-20T00:00:00Z","timestamp":1642636800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32070572"],"award-info":[{"award-number":["32070572"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Data"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Bacterial integrative and conjugative elements (ICEs) are highly modular mobile genetic elements critical to the horizontal transfer of antibiotic resistance and virulence factor genes. To better understand and analyze the ongoing increase of ICEs, we developed an Integrative and Conjugative Element Ontology (ICEO) to represent the gene components, functional modules, and other information of experimentally verified ICEs. ICEO is aligned with the upper-level Basic Formal Ontology and reuses existing reliable ontologies. There are 31,081 terms, including 26,814 classes from 14 ontologies and 4128 ICEO-specific classes, representing the information of 271 known experimentally verified ICEs from 235 bacterial strains in ICEO currently and 311 predicted ICEs of 272 completely sequenced <jats:italic>Klebsiella pneumoniae<\/jats:italic> strains. Three ICEO use cases were illustrated to investigate complex joins of ICEs and their harboring antibiotic resistance or virulence factor genes by using SPARQL or DL query. ICEO has been approved as an Open Biomedical Ontology library ontology. It may be dedicated to facilitating systematical ICE knowledge representation, integration, and computer-assisted queries.<\/jats:p>","DOI":"10.1038\/s41597-021-01112-5","type":"journal-article","created":{"date-parts":[[2022,1,20]],"date-time":"2022-01-20T11:05:12Z","timestamp":1642676712000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["ICEO, a biological ontology for representing and analyzing bacterial integrative and conjugative elements"],"prefix":"10.1038","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3781-6962","authenticated-orcid":false,"given":"Meng","family":"Liu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jialin","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guitian","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoli","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0724-3390","authenticated-orcid":false,"given":"Zixin","family":"Deng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9189-9661","authenticated-orcid":false,"given":"Yongqun","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hong-Yu","family":"Ou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,1,20]]},"reference":[{"key":"1112_CR1","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1046\/j.1365-2958.2002.03191.x","volume":"46","author":"V Burrus","year":"2002","unstructured":"Burrus, V., Pavlovic, G., Decaris, B. & Gu\u00e9don, G. Conjugative transposons: the tip of the iceberg. Mol. Microbiol. 46, 601\u2013610 (2002).","journal-title":"Mol. Microbiol."},{"key":"1112_CR2","doi-asserted-by":"publisher","first-page":"552","DOI":"10.1038\/nrmicro2382","volume":"8","author":"RA Wozniak","year":"2010","unstructured":"Wozniak, R. A. & Waldor, M. K. Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat. Rev. Microbiol. 8, 552\u201363 (2010).","journal-title":"Nat. Rev. Microbiol."},{"key":"1112_CR3","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1146\/annurev-genet-112414-055018","volume":"49","author":"CM Johnson","year":"2015","unstructured":"Johnson, C. M. & Grossman, A. D. Integrative and conjugative elements (ICEs): what they do and how they work. Annu Rev Genet 49, 577\u2013601 (2015).","journal-title":"Annu Rev Genet"},{"key":"1112_CR4","doi-asserted-by":"publisher","first-page":"512","DOI":"10.1093\/femsre\/fux008","volume":"41","author":"F Delavat","year":"2017","unstructured":"Delavat, F., Miyazaki, R., Carraro, N., Pradervand, N. & van der Meer, J. R. The hidden life of integrative and conjugative elements. FEMS Microbiol. Rev. 41, 512\u2013537 (2017).","journal-title":"FEMS Microbiol. Rev."},{"key":"1112_CR5","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.mib.2017.03.014","volume":"38","author":"V Burrus","year":"2017","unstructured":"Burrus, V. Mechanisms of stabilization of integrative and conjugative elements. Curr. Opin. Microbiol. 38, 44\u201350 (2017).","journal-title":"Curr. Opin. Microbiol."},{"key":"1112_CR6","doi-asserted-by":"publisher","first-page":"D660","DOI":"10.1093\/nar\/gky1123","volume":"47","author":"M Liu","year":"2019","unstructured":"Liu, M. et al. ICEberg 2.0: an updated database of bacterial integrative and conjugative elements. Nucleic Acids Res. 47, D660\u2013D665 (2019).","journal-title":"Nucleic Acids Res."},{"key":"1112_CR7","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/j.mib.2018.04.004","volume":"45","author":"KL Wyres","year":"2018","unstructured":"Wyres, K. L. & Holt, K. E. Klebsiella pneumoniae as a key trafficker of drug resistance genes from environmental to clinically important bacteria. Curr. Opin. Microbiol. 45, 131\u2013139 (2018).","journal-title":"Curr. Opin. Microbiol."},{"key":"1112_CR8","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.tim.2020.05.011","volume":"29","author":"J Botelho","year":"2020","unstructured":"Botelho, J. & Schulenburg, H. The role of integrative and conjugative elements in antibiotic resistance evolution. Trends Microbiol. 29, 8\u201318 (2020).","journal-title":"Trends Microbiol."},{"key":"1112_CR9","doi-asserted-by":"publisher","first-page":"2770","DOI":"10.1093\/jac\/dkv204","volume":"70","author":"D Bi","year":"2015","unstructured":"Bi, D. et al. Mapping the resistance-associated mobilome of a carbapenem-resistant Klebsiella pneumoniae strain reveals insights into factors shaping these regions and facilitates generation of a \u2018resistance-disarmed\u2019 model organism. J. Antimicrob. Chemother. 70, 2770\u20134 (2015).","journal-title":"J. Antimicrob. Chemother."},{"key":"1112_CR10","doi-asserted-by":"publisher","first-page":"e000196","DOI":"10.1099\/mgen.0.000196","volume":"4","author":"MMC Lam","year":"2018","unstructured":"Lam, M. M. C. et al. Genetic diversity, mobilisation and spread of the yersiniabactin-encoding mobile element ICEKp in Klebsiella pneumoniae populations. Microb. Genomics 4, e000196 (2018).","journal-title":"Microb. Genomics"},{"key":"1112_CR11","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1128\/JB.01219-07","volume":"190","author":"T-L Lin","year":"2008","unstructured":"Lin, T.-L., Lee, C.-Z., Hsieh, P.-F., Tsai, S.-F. & Wang, J.-T. Characterization of integrative and conjugative element ICEKp1-associated genomic heterogeneity in a Klebsiella pneumoniae strain isolated from a primary liver abscess. J. Bacteriol. 190, 515\u2013526 (2008).","journal-title":"J. Bacteriol."},{"key":"1112_CR12","doi-asserted-by":"publisher","first-page":"722","DOI":"10.1038\/nrmicro1235","volume":"3","author":"LS Frost","year":"2005","unstructured":"Frost, L. S., Leplae, R., Summers, A. O. & Toussaint, A. Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3, 722\u2013732 (2005).","journal-title":"Nat. Rev. Microbiol."},{"key":"1112_CR13","doi-asserted-by":"publisher","first-page":"1251","DOI":"10.1038\/nbt1346","volume":"25","author":"B Smith","year":"2007","unstructured":"Smith, B. et al. The OBO Foundry: coordinated evolution of ontologies to support biomedical data integration. Nat. Biotechnol. 25, 1251\u20135 (2007).","journal-title":"Nat. Biotechnol."},{"key":"1112_CR14","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1093\/bib\/bbl027","volume":"7","author":"O Bodenreider","year":"2006","unstructured":"Bodenreider, O. & Stevens, R. Bio-ontologies: current trends and future directions. Brief. Bioinform. 7, 256\u2013274 (2006).","journal-title":"Brief. Bioinform."},{"key":"1112_CR15","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.1093\/bib\/bbv011","volume":"16","author":"R Hoehndorf","year":"2015","unstructured":"Hoehndorf, R., Schofield, P. N. & Gkoutos, G. V. The role of ontologies in biological and biomedical research: a functional perspective. Brief. Bioinform. 16, 1069\u20131080 (2015).","journal-title":"Brief. Bioinform."},{"key":"1112_CR16","doi-asserted-by":"publisher","first-page":"D865","DOI":"10.1093\/nar\/gkw1039","volume":"45","author":"S K\u00f6hler","year":"2017","unstructured":"K\u00f6hler, S. et al. The human phenotype ontology in 2017. Nucleic Acids Res. 45, D865\u2013D876 (2017).","journal-title":"Nucleic Acids Res."},{"key":"1112_CR17","doi-asserted-by":"publisher","first-page":"1452","DOI":"10.1056\/NEJMra1615014","volume":"379","author":"MA Haendel","year":"2018","unstructured":"Haendel, M. A., Chute, C. G. & Robinson, P. N. Classification, ontology, and precision medicine. N. Engl. J. Med. 379, 1452\u20131462 (2018).","journal-title":"N. Engl. J. Med."},{"key":"1112_CR18","doi-asserted-by":"publisher","first-page":"D330","DOI":"10.1093\/nar\/gky1055","volume":"47","author":"The Gene Ontology Consortium.","year":"2019","unstructured":"The Gene Ontology Consortium. The Gene Ontology Resource: 20 years and still GOing strong. Nucleic Acids Res. 47, D330\u2013D338 (2019).","journal-title":"Nucleic Acids Res."},{"key":"1112_CR19","doi-asserted-by":"publisher","DOI":"10.1186\/s13326-017-0169-2","volume":"9","author":"Y He","year":"2018","unstructured":"He, Y. et al. The eXtensible ontology development (XOD) principles and tool implementation to support ontology interoperability. J. Biomed. Semant. 9, 3 (2018).","journal-title":"J. Biomed. Semant."},{"key":"1112_CR20","doi-asserted-by":"crossref","unstructured":"Arp, R., Smith, B. & Spear, A. Building Ontologies using basic formal ontology. Camb. MA USA (2015).","DOI":"10.7551\/mitpress\/9780262527811.001.0001"},{"key":"1112_CR21","unstructured":"He, Y., Liu, Y. & Zhao, B. OGG: a biological ontology for representing genes and genomes in specific organisms. in ICBO 13\u201320 (Citeseer, 2014)."},{"key":"1112_CR22","doi-asserted-by":"publisher","first-page":"D8","DOI":"10.1093\/nar\/gkx1095","volume":"46","author":"NCBI Resource Coordinators.","year":"2018","unstructured":"NCBI Resource Coordinators. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 46, D8\u2013D13 (2018).","journal-title":"Nucleic Acids Res."},{"key":"1112_CR23","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/gb-2005-6-9-119","volume":"6","author":"B Smith","year":"2005","unstructured":"Smith, B. et al. Relations in biomedical ontologies. Genome Biol. 6, 1\u201315 (2005).","journal-title":"Genome Biol."},{"key":"1112_CR24","doi-asserted-by":"publisher","first-page":"4492","DOI":"10.1128\/JB.00315-09","volume":"191","author":"K-M Wu","year":"2009","unstructured":"Wu, K.-M. et al. Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitis. J. Bacteriol. 191, 4492\u20134501 (2009).","journal-title":"J. Bacteriol."},{"key":"1112_CR25","doi-asserted-by":"publisher","first-page":"D347","DOI":"10.1093\/nar\/gkw918","volume":"45","author":"E Ong","year":"2017","unstructured":"Ong, E. et al. Ontobee: a linked ontology data server to support ontology term dereferencing, linkage, query and integration. Nucleic Acids Res. 45, D347\u2013D352 (2017).","journal-title":"Nucleic Acids Res."},{"key":"1112_CR26","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1093\/jac\/dkx337","volume":"73","author":"J Botelho","year":"2018","unstructured":"Botelho, J., Grosso, F. & Peixe, L. Unravelling the genome of a Pseudomonas aeruginosa isolate belonging to the high-risk clone ST235 reveals an integrative conjugative element housing a blaGES-6 carbapenemase. J. Antimicrob. Chemother. 73, 77\u201383 (2018).","journal-title":"J. Antimicrob. Chemother."},{"key":"1112_CR27","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1016\/j.jgar.2020.08.002","volume":"23","author":"Z Li","year":"2020","unstructured":"Li, Z. et al. Genetic characterisation of a complex class 1 integron in an NDM-1-producing Citrobacter freundii ST396 clinical strain isolated from a urine sample. J. Glob. Antimicrob. Resist. 23, 64\u201366 (2020).","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"1112_CR28","doi-asserted-by":"publisher","first-page":"W81","DOI":"10.1093\/nar\/gkz310","volume":"47","author":"K Blin","year":"2019","unstructured":"Blin, K. et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res. 47, W81\u2013W87 (2019).","journal-title":"Nucleic Acids Res."},{"key":"1112_CR29","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1007\/s10462-011-9251-9","volume":"38","author":"C Martinez-Cruz","year":"2012","unstructured":"Martinez-Cruz, C., Blanco, I. J. & Vila, M. A. Ontologies versus relational databases: are they so different? A comparison. Artif. Intell. Rev. 38, 271\u2013290 (2012).","journal-title":"Artif. Intell. Rev."},{"key":"1112_CR30","doi-asserted-by":"publisher","DOI":"10.1186\/2041-1480-3-18","volume":"3","author":"J Hur","year":"2012","unstructured":"Hur, J., Ozgur, A., Xiang, Z. & He, Y. Identification of fever and vaccine-associated gene interaction networks using ontology-based literature mining. J Biomed Semant. 3, 18 (2012).","journal-title":"J Biomed Semant."},{"key":"1112_CR31","doi-asserted-by":"publisher","DOI":"10.1186\/2041-1480-6-2","volume":"6","author":"J Hur","year":"2015","unstructured":"Hur, J., \u00d6zg\u00fcr, A., Xiang, Z. & He, Y. Development and application of an interaction network ontology for literature mining of vaccine-associated gene-gene interactions. J. Biomed. Semant. 6, 2 (2015).","journal-title":"J. Biomed. Semant."},{"key":"1112_CR32","doi-asserted-by":"publisher","first-page":"D45","DOI":"10.1093\/nar\/gkh084","volume":"32","author":"R Leplae","year":"2004","unstructured":"Leplae, R., Hebrant, A., Wodak, S. J. & Toussaint, A. ACLAME: A CLAssification of Mobile genetic Elements. Nucleic Acids Res. 32, D45\u2013D49 (2004).","journal-title":"Nucleic Acids Res."},{"key":"1112_CR33","doi-asserted-by":"publisher","first-page":"567","DOI":"10.1016\/j.resmic.2007.05.002","volume":"158","author":"A Toussaint","year":"2007","unstructured":"Toussaint, A., Lima-Mendez, G. & Leplae, R. PhiGO, a phage ontology associated with the ACLAME database. Res. Microbiol. 158, 567\u201371 (2007).","journal-title":"Res. Microbiol."},{"key":"1112_CR34","doi-asserted-by":"publisher","first-page":"D57","DOI":"10.1093\/nar\/gkp938","volume":"38","author":"R Leplae","year":"2010","unstructured":"Leplae, R., Lima-Mendez, G. & Toussaint, A. ACLAME: A CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res. 38, D57\u2013D61 (2010).","journal-title":"Nucleic Acids Res."},{"key":"1112_CR35","doi-asserted-by":"publisher","first-page":"4839","DOI":"10.1128\/AEM.00167-06","volume":"72","author":"A Raynal","year":"2006","unstructured":"Raynal, A., Karray, F., Tuphile, K., Darbon-Rong\u00e8re, E. & Pernodet, J.-L. Excisable Cassettes: New Tools for Functional Analysis of Streptomyces Genomes. Appl. Environ. Microbiol. 72, 4839\u20134844 (2006).","journal-title":"Appl. Environ. Microbiol."},{"key":"1112_CR36","doi-asserted-by":"publisher","DOI":"10.1038\/sdata.2016.18","volume":"3","author":"MD Wilkinson","year":"2016","unstructured":"Wilkinson, M. D. et al. The FAIR guiding principles for scientific data management and stewardship. Sci. Data 3, 160018 (2016).","journal-title":"Sci. Data"},{"key":"1112_CR37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13326-017-0172-7","volume":"9","author":"N Matentzoglu","year":"2018","unstructured":"Matentzoglu, N., Malone, J., Mungall, C. & Stevens, R. MIRO: guidelines for minimum information for the reporting of an ontology. J. Biomed. Semant. 9, 1\u201313 (2018).","journal-title":"J. Biomed. Semant."},{"key":"1112_CR38","doi-asserted-by":"publisher","DOI":"10.1186\/1756-0500-3-175","volume":"3","author":"Z Xiang","year":"2010","unstructured":"Xiang, Z., Courtot, M., Brinkman, R. R., Ruttenberg, A. & He, Y. OntoFox: web-based support for ontology reuse. BMC Res Notes 3, 175 (2010).","journal-title":"BMC Res Notes"},{"key":"1112_CR39","unstructured":"Murphy M. et al. Gene Help: Integrated Access to Genes of Genomes in the Reference Sequence Collection. (National Center for Biotechnology Information (US), 2019)."},{"key":"1112_CR40","doi-asserted-by":"publisher","DOI":"10.1186\/2041-1480-6-4","volume":"6","author":"Z Xiang","year":"2015","unstructured":"Xiang, Z., Zheng, J., Lin, Y. & He, Y. Ontorat: automatic generation of new ontology terms, annotations, and axioms based on ontology design patterns. J. Biomed. Semant. 6, 4 (2015).","journal-title":"J. Biomed. Semant."},{"key":"1112_CR41","doi-asserted-by":"publisher","DOI":"10.1186\/s13326-017-0126-0","volume":"8","author":"D Osumi-Sutherland","year":"2017","unstructured":"Osumi-Sutherland, D., Courtot, M., Balhoff, J. P. & Mungall, C. Dead simple OWL design patterns. J. Biomed. Semant. 8, 18 (2017).","journal-title":"J. Biomed. Semant."},{"key":"1112_CR42","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1145\/2757001.2757003","volume":"1","author":"MA Musen","year":"2015","unstructured":"Musen, M. A. The Prot\u00e9g\u00e9 project: a look back and a look forward. AI Matters 1, 4\u201312 (2015).","journal-title":"AI Matters"},{"key":"1112_CR43","doi-asserted-by":"publisher","first-page":"1882","DOI":"10.1109\/TSMCB.2012.2234739","volume":"43","author":"A Scalmato","year":"2013","unstructured":"Scalmato, A., Sgorbissa, A. & Zaccaria, R. Describing and recognizing patterns of events in smart environments with Description Logic. IEEE Trans. Cybern. 43, 1882\u20131897 (2013).","journal-title":"IEEE Trans. Cybern."},{"key":"1112_CR44","doi-asserted-by":"publisher","DOI":"10.6084\/m9.figshare.17008543.v2","author":"L Meng","year":"2021","unstructured":"Meng, L. ICEs info. figshare https:\/\/doi.org\/10.6084\/m9.figshare.17008543.v2 (2021)."}],"container-title":["Scientific Data"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41597-021-01112-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41597-021-01112-5","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41597-021-01112-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,24]],"date-time":"2022-11-24T20:04:24Z","timestamp":1669320264000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41597-021-01112-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,20]]},"references-count":44,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["1112"],"URL":"https:\/\/doi.org\/10.1038\/s41597-021-01112-5","relation":{"references":[{"id-type":"doi","id":"10.6084\/m9.figshare.17008543.v2","asserted-by":"subject"}]},"ISSN":["2052-4463"],"issn-type":[{"value":"2052-4463","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,20]]},"assertion":[{"value":"14 July 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 December 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 January 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"11"}}