{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T10:38:24Z","timestamp":1790851104755,"version":"4.1.0"},"reference-count":65,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,11,8]],"date-time":"2017-11-08T00:00:00Z","timestamp":1510099200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,11,8]],"date-time":"2017-11-08T00:00:00Z","timestamp":1510099200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p><jats:italic>Campylobacter fetus<\/jats:italic> is a venereal pathogen of cattle and sheep, and an opportunistic human pathogen. It is often assumed that <jats:italic>C. fetus<\/jats:italic> infection occurs in humans as a zoonosis through food chain transmission. Here we show that mammalian <jats:italic>C. fetus<\/jats:italic> consists of distinct evolutionary lineages, primarily associated with either human or bovine hosts. We use whole-genome phylogenetics on 182 strains from 17 countries to provide evidence that <jats:italic>C. fetus<\/jats:italic> may have originated in humans around 10,500 years ago and may have \u201cjumped\u201d into cattle during the livestock domestication period. We detect <jats:italic>C. fetus<\/jats:italic> genomes in 8% of healthy human fecal metagenomes, where the human-associated lineages are the dominant type (78%). Thus, our work suggests that <jats:italic>C. fetus<\/jats:italic> is an unappreciated human intestinal pathobiont likely spread by human to human transmission. This genome-based evolutionary framework will facilitate <jats:italic>C. fetus<\/jats:italic> epidemiology research and the development of improved molecular diagnostics and prevention schemes for this neglected pathogen.<\/jats:p>","DOI":"10.1038\/s41467-017-01449-9","type":"journal-article","created":{"date-parts":[[2017,11,3]],"date-time":"2017-11-03T06:38:24Z","timestamp":1509691104000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":50,"title":["Distinct Campylobacter fetus lineages adapted as livestock pathogens and human pathobionts in the intestinal microbiota"],"prefix":"10.1038","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6516-3404","authenticated-orcid":false,"given":"Gregorio","family":"Iraola","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4144-2537","authenticated-orcid":false,"given":"Samuel C.","family":"Forster","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nitin","family":"Kumar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philippe","family":"Lehours","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sadjia","family":"Bekal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francisco J.","family":"Garc\u00eda-Pe\u00f1a","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fernando","family":"Paolicchi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia","family":"Morsella","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2413-296X","authenticated-orcid":false,"given":"Helmut","family":"Hotzel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Po-Ren","family":"Hsueh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"Vidal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simon","family":"L\u00e9vesque","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wataru","family":"Yamazaki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1203-8017","authenticated-orcid":false,"given":"Claudia","family":"Balzan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agueda","family":"Vargas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6207-4721","authenticated-orcid":false,"given":"Alessandra","family":"Piccirillo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bonnie","family":"Chaban","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janet E.","family":"Hill","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Betancor","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7140-4219","authenticated-orcid":false,"given":"Luis","family":"Collado","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabelle","family":"Truyers","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne C.","family":"Midwinter","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hatice T.","family":"Dagi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francis","family":"M\u00e9graud","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luc\u00eda","family":"Calleros","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruben","family":"P\u00e9rez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6982-4399","authenticated-orcid":false,"given":"Hugo","family":"Naya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Trevor D.","family":"Lawley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,11,8]]},"reference":[{"key":"1449_CR1","doi-asserted-by":"publisher","first-page":"e221","DOI":"10.1111\/j.1439-0531.2008.01218.x","volume":"45","author":"GD Mshelia","year":"2010","unstructured":"Mshelia, G. D., Amin, J. D., Woldehiwet, Z., Murray, R. D. & Egwu, G. O. Epidemiology of bovine venereal campylobacteriosis: geographic distribution and recent advances in molecular diagnostic techniques. Reprod. Domest. Anim. \n                           45, e221\u2013e230 (2010).","journal-title":"Reprod. Domest. Anim."},{"key":"1449_CR2","doi-asserted-by":"publisher","first-page":"1579","DOI":"10.1093\/cid\/ciu085","volume":"58","author":"JA Wagenaar","year":"2014","unstructured":"Wagenaar, J. A. et al. Campylobacter fetus infections in humans: exposure and disease. Clin. Infect. Dis. \n                           58, 1579\u20131586 (2014).","journal-title":"Clin. Infect. Dis."},{"key":"1449_CR3","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1097\/MD.0b013e3181f2638d","volume":"89","author":"A Fern\u00e1ndez-Cruz","year":"2010","unstructured":"Fern\u00e1ndez-Cruz, A. et al. Campylobacter bacteremia: clinical characteristics, incidence, and outcome over 23 years. Medicine \n                           89, 319\u2013330 (2010).","journal-title":"Medicine"},{"key":"1449_CR4","doi-asserted-by":"publisher","first-page":"2944","DOI":"10.1099\/ijs.0.057778-0","volume":"64","author":"C Fitzgerald","year":"2014","unstructured":"Fitzgerald, C. et al. Campylobacter fetus subsp. testudinum subsp. nov., isolated from humans and reptiles. Int. J. Sys. Evol. Microbiol. \n                           64, 2944\u20132948 (2014).","journal-title":"Int. J. Sys. Evol. Microbiol."},{"key":"1449_CR5","doi-asserted-by":"publisher","DOI":"10.1007\/s10096-015-2393-y","volume":"34","author":"G Iraola","year":"2015","unstructured":"Iraola, G. et al. A rural worker infected with a bovine-prevalent genotype of Campylobacter fetus subsp. fetus supports zoonotic transmission and inconsistency of MLST and whole-genome typing. Eur. J. Clin. Microbiol. Infect. Dis. \n                           34, 1593 (2015).","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"1449_CR6","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1128\/JCM.01439-09","volume":"48","author":"KE Dingle","year":"2010","unstructured":"Dingle, K. E. et al. Genetic relationships among reptilian and mammalian Campylobacter fetus strains determined by multilocus sequence typing. J. Clin. Microbiol. \n                           48, 977\u2013980 (2010).","journal-title":"J. Clin. Microbiol."},{"key":"1449_CR7","doi-asserted-by":"publisher","first-page":"2006","DOI":"10.1093\/gbe\/evw146","volume":"8","author":"MJ Gilbert","year":"2016","unstructured":"Gilbert, M. J. et al. Comparative genomics of Campylobacter fetus from reptiles and mammals reveals divergent evolution in host-associated lineages. Genome Biol. Evol. \n                           8, 2006\u20132019 (2016).","journal-title":"Genome Biol. Evol."},{"key":"1449_CR8","doi-asserted-by":"publisher","first-page":"4183","DOI":"10.1128\/JCM.01837-14","volume":"52","author":"L van der Graaf-van Bloois","year":"2014","unstructured":"van der Graaf-van Bloois, L. et al. Inconsistency of phenotypic and genomic characteristics of Campylobacter fetus subspecies requires reevaluation of current diagnostics. J. Clin. Microbiol. \n                           52, 4183\u20134188 (2014).","journal-title":"J. Clin. Microbiol."},{"key":"1449_CR9","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-016-3058-7","volume":"17","author":"L van der Graaf-van Bloois","year":"2016","unstructured":"van der Graaf-van Bloois, L. et al. Whole genome sequence analysis indicates recent diversification of mammal-associated Campylobacter fetus and implicates a genetic factor associated with H2S production. BMC Genomics \n                           17, 713 (2016).","journal-title":"BMC Genomics"},{"key":"1449_CR10","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1099\/ijs.0.64483-0","volume":"57","author":"J Goris","year":"2007","unstructured":"Goris, J. et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Sys. Evol. Microbiol. \n                           57, 81\u201391 (2007).","journal-title":"Int. J. Sys. Evol. Microbiol."},{"key":"1449_CR11","doi-asserted-by":"publisher","first-page":"1224","DOI":"10.1093\/molbev\/mst028","volume":"30","author":"L Cheng","year":"2013","unstructured":"Cheng, L., Connor, T. R., Sir\u00e9n, J., Aanensen, D. M. & Corander, J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol. Biol. Evol. \n                           30, 1224\u20131228 (2013).","journal-title":"Mol. Biol. Evol."},{"key":"1449_CR12","doi-asserted-by":"publisher","first-page":"785","DOI":"10.1111\/1755-0998.12352","volume":"15","author":"D Duch\u00eane","year":"2015","unstructured":"Duch\u00eane, D., Duch\u00eane, S. & Ho, S. Y. W. Tree imbalance causes a bias in phylogenetic estimation of evolutionary timescales using heterochronous sequences. Mol. Ecol. Res. \n                           15, 785\u2013794 (2015).","journal-title":"Mol. Ecol. Res."},{"key":"1449_CR13","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1111\/2041-210X.12466","volume":"7","author":"GGR Murray","year":"2016","unstructured":"Murray, G. G. R. et al. The effect of genetic structure on molecular dating and tests for temporal signal. Methods Ecol. Evol. \n                           7, 80\u201389 (2016).","journal-title":"Methods Ecol. Evol."},{"key":"1449_CR14","doi-asserted-by":"publisher","first-page":"3087","DOI":"10.1111\/j.1365-294X.2011.05178.x","volume":"20","author":"SY Ho","year":"2011","unstructured":"Ho, S. Y. et al. Time-dependent rates of molecular evolution. Mol. Ecol. \n                           20, 3087\u20133101 (2011).","journal-title":"Mol. Ecol."},{"key":"1449_CR15","doi-asserted-by":"publisher","first-page":"721","DOI":"10.1038\/ismej.2015.149","volume":"10","author":"BL Dearlove","year":"2016","unstructured":"Dearlove, B. L. et al. Rapid host switching in generalist Campylobacter strains erodes the signal for tracing human infections. ISME J. \n                           10, 721\u2013729 (2016).","journal-title":"ISME J."},{"key":"1449_CR16","volume":"2","author":"S Duch\u00eane","year":"2016","unstructured":"Duch\u00eane, S. et al. Genome-scale rates of evolutionary change in bacteria. Microb. Genom. \n                           2, 11 (2016).","journal-title":"Microb. Genom."},{"key":"1449_CR17","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1016\/j.meegid.2007.08.001","volume":"8","author":"J Parker","year":"2008","unstructured":"Parker, J., Rambaut, A. & Pybus, O. G. Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect. Genet. Evol. \n                           8, 239\u2013246 (2008).","journal-title":"Infect. Genet. Evol."},{"key":"1449_CR18","doi-asserted-by":"publisher","first-page":"2757","DOI":"10.1073\/pnas.91.7.2757","volume":"99","author":"RT Loftus","year":"1994","unstructured":"Loftus, R. T. et al. Evidence for two independent domestications of cattle. Proc. Natl Acad. Sci. USA \n                           99, 2757\u20132761 (1994).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1449_CR19","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-015-2087-y","volume":"16","author":"A Baig","year":"2015","unstructured":"Baig, A. et al. Genetic import and phenotype specific alleles associated with hyper-invasion in Campylobacter jejuni. BMC Genomics \n                           16, 852 (2015).","journal-title":"BMC Genomics"},{"key":"1449_CR20","doi-asserted-by":"publisher","first-page":"4714","DOI":"10.1128\/JB.186.14.4714-4729.2004","volume":"186","author":"K Palyada","year":"2004","unstructured":"Palyada, K., Threadgill, D. & Stintzi, A. Iron acquisition and regulation in Campylobacter jejuni. J. Bacteriol. \n                           186, 4714\u20134729 (2004).","journal-title":"J. Bacteriol."},{"key":"1449_CR21","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0152832","volume":"11","author":"L van der Graaf-van Bloois","year":"2016","unstructured":"van der Graaf-van Bloois, L. et al. Campylobacter fetus subspecies contain conserved type IV secretion systems on multiple genomic islands and plasmids. PloS ONE \n                           11, e0152832 (2016).","journal-title":"PloS ONE"},{"key":"1449_CR22","doi-asserted-by":"publisher","first-page":"2392","DOI":"10.1093\/gbe\/evu195","volume":"6","author":"G Iraola","year":"2014","unstructured":"Iraola, G. et al. Genomic evidence for the emergence and evolution of pathogenicity and niche preferences in the genus Campylobacter. Genome Biol. Evol. \n                           6, 2392\u20132405 (2014).","journal-title":"Genome Biol. Evol."},{"key":"1449_CR23","doi-asserted-by":"publisher","first-page":"9300","DOI":"10.1073\/pnas.0409873102","volume":"102","author":"S Brandt","year":"2005","unstructured":"Brandt, S. NF-kB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc. Natl Acad. Sci. USA \n                           102, 9300\u20139305 (2005).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1449_CR24","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1016\/j.mimet.2016.11.012","volume":"132","author":"L Calleros","year":"2017","unstructured":"Calleros, L. et al. Assessing the intra-species genetic variability in the clonal pathogen Campylobacter fetus: CRISPRs are highly polymorphic DNA markers. J. Microbiol. Methods \n                           132, 86\u201394 (2017).","journal-title":"J. Microbiol. Methods"},{"key":"1449_CR25","first-page":"53","volume":"77","author":"V Kommireddy","year":"2009","unstructured":"Kommireddy, V. & Nagaraja, V. Diverse functions of restriction-modification systems in addition to cellular defense. Mol. Biol. Rev. \n                           77, 53\u201372 (2009).","journal-title":"Mol. Biol. Rev."},{"key":"1449_CR26","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1046\/j.1365-2672.2003.01969.x","volume":"95","author":"CM Logue","year":"2003","unstructured":"Logue, C. M. et al. The incidence of Campylobacter spp. on processed turkey from processing plants in the midwestern United States. J. Appl. Microbiol. \n                           95, 234\u2013241 (2003).","journal-title":"J. Appl. Microbiol."},{"key":"1449_CR27","doi-asserted-by":"publisher","first-page":"1277","DOI":"10.1099\/jmm.0.46628-0","volume":"55","author":"I Kempf","year":"2006","unstructured":"Kempf, I. et al. Broilers do not play a dominant role in the Campylobacter fetus contamination of humans. J. Med. Microbiol. \n                           55, 1277\u20131278 (2006).","journal-title":"J. Med. Microbiol."},{"key":"1449_CR28","doi-asserted-by":"publisher","first-page":"D604","DOI":"10.1093\/nar\/gkv1216","volume":"44","author":"S Forster","year":"2016","unstructured":"Forster, S. et al. HPMCD: the database of human microbial communities from metagenomic datasets and microbial reference genomes. Nucleic Acids Res. \n                           44, D604\u2013D609 (2016).","journal-title":"Nucleic Acids Res."},{"key":"1449_CR29","doi-asserted-by":"publisher","DOI":"10.1093\/ofid\/ofw172.901","volume":"3","author":"X Marchand-Sen\u00e9cal","year":"2016","unstructured":"Marchand-Sen\u00e9cal, X., Bekal, S., Pilon, P. A., Sylvestre, J.-L. & Gaudreau, C. Campylobacter fetus outbreak in Montreal, Quebec, Canada: a retrospective analysis. Open Forum Infect. Dis. \n                           3, S357 (2016).","journal-title":"Open Forum Infect. Dis."},{"key":"1449_CR30","doi-asserted-by":"publisher","first-page":"454","DOI":"10.1093\/gbe\/evq031","volume":"2","author":"CM Guinane","year":"2010","unstructured":"Guinane, C. M. et al. Evolutionary genomics of Staphylococcus aureus reveals insights into the origin and molecular basis of ruminant host adaptation. Genome Biol. Evol. \n                           2, 454\u2013466 (2010).","journal-title":"Genome Biol. Evol."},{"key":"1449_CR31","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1016\/j.tim.2016.11.012","volume":"25","author":"MQ Carter","year":"2017","unstructured":"Carter, M. Q. Decoding the ecological function of accessory genome. Trends Microbiol. \n                           25, 6\u20138 (2017).","journal-title":"Trends Microbiol."},{"key":"1449_CR32","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms9924","volume":"6","author":"R Niehus","year":"2015","unstructured":"Niehus, R., Mitri, S., Fletcher, A. G. & Foster, K. R. Migration and horizontal gene transfer divide microbial genomes into multiple niches. Nat. Commun. \n                           6, 8924 (2015).","journal-title":"Nat. Commun."},{"key":"1449_CR33","doi-asserted-by":"publisher","DOI":"10.1038\/nmicrobiol.2017.40","volume":"2","author":"JO McInerney","year":"2016","unstructured":"McInerney, J. O., McNally, A. & O\u2019Connell, J. O. Why prokaryotes have pangenomes. Nat. Microbiol. \n                           2, 17040 (2016).","journal-title":"Nat. Microbiol."},{"key":"1449_CR34","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1038\/ng.2478","volume":"45","author":"M He","year":"2013","unstructured":"He, M. et al. Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nat. Genet. \n                           45, 109\u2013113 (2013).","journal-title":"Nat. Genet."},{"key":"1449_CR35","volume":"2","author":"AJ Page","year":"2016","unstructured":"Page, A. J. et al. Robust high-throughput prokaryote de novo assembly and improvement pipeline for Illumina data. Microb. Genome \n                           2, e000083 (2016).","journal-title":"Microb. Genome"},{"key":"1449_CR36","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2014-15-3-r46","volume":"15","author":"DE Wood","year":"2014","unstructured":"Wood, D. E. & Salzberg, S. L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. \n                           15, R46 (2014).","journal-title":"Genome Biol."},{"key":"1449_CR37","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1101\/gr.074492.107","volume":"18","author":"DR Zerbino","year":"2008","unstructured":"Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. \n                           18, 821\u2013829 (2008).","journal-title":"Genome Res."},{"key":"1449_CR38","unstructured":"Gladman, S. & Seemann, T. VelvetOptimiser. https:\/\/github.com\/tseemann\/VelvetOptimiser (2008)."},{"key":"1449_CR39","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1093\/bioinformatics\/btq683","volume":"27","author":"M Boetzer","year":"2010","unstructured":"Boetzer, M., Henkel, C. V., Jansen, H. J., Butler, D. & Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics \n                           27, 578\u2013579 (2010).","journal-title":"Bioinformatics"},{"key":"1449_CR40","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-13-S14-S8","volume":"13","author":"F Nadalin","year":"2012","unstructured":"Nadalin, F., Vezzi, F. & Pollcriti, A. GapFiller: a de novo assembly approach to fill the gap within paired reads. BMC Bioinformatics \n                           13, S8 (2012).","journal-title":"BMC Bioinformatics"},{"key":"1449_CR41","unstructured":"Ponstingl, H. & Ning, Z. SMALT. http:\/\/www.sanger.ac.uk\/science\/tools\/smalt-0. (2015)."},{"key":"1449_CR42","doi-asserted-by":"publisher","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","volume":"30","author":"T Seemann","year":"2014","unstructured":"Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics \n                           30, 2068\u20132069 (2014).","journal-title":"Bioinformatics"},{"key":"1449_CR43","doi-asserted-by":"publisher","first-page":"3468","DOI":"10.1099\/ijsem.0.001219","volume":"66","author":"A Piccirillo","year":"2016","unstructured":"Piccirillo, A. et al. Campylobacter geochelonis sp. nov., isolated from the western Hermann\u2019s tortoise (Testudo hermanni hermanni). Int. J. Sys. Evol. Microbiol. \n                           66, 3468\u20133476 (2016).","journal-title":"Int. J. Sys. Evol. Microbiol."},{"key":"1449_CR44","doi-asserted-by":"publisher","first-page":"3691","DOI":"10.1093\/bioinformatics\/btv421","volume":"31","author":"AJ Page","year":"2015","unstructured":"Page, A. J. et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics \n                           31, 3691\u20133693 (2015).","journal-title":"Bioinformatics"},{"key":"1449_CR45","doi-asserted-by":"publisher","first-page":"1658","DOI":"10.1093\/bioinformatics\/btl158","volume":"22","author":"W Li","year":"2006","unstructured":"Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics \n                           22, 1658\u20131659 (2006).","journal-title":"Bioinformatics"},{"key":"1449_CR46","doi-asserted-by":"publisher","first-page":"1575","DOI":"10.1093\/nar\/30.7.1575","volume":"30","author":"AJ Enright","year":"2002","unstructured":"Enright, A. J., Van Dongen, S. & Ouzonis, C. A. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. \n                           30, 1575\u20131584 (2002).","journal-title":"Nucleic Acids Res."},{"key":"1449_CR47","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gku1196","volume":"43","author":"NJ Croucher","year":"2015","unstructured":"Croucher, N. J. et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. \n                           43, e15 (2015).","journal-title":"Nucleic Acids Res."},{"key":"1449_CR48","doi-asserted-by":"publisher","first-page":"1969","DOI":"10.1093\/molbev\/mss075","volume":"29","author":"AJ Drummond","year":"2012","unstructured":"Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with beauti and the beast 1.7. Mol. Biol. Evol. \n                           29, 1969\u20131973 (2012).","journal-title":"Mol. Biol. Evol."},{"key":"1449_CR49","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1093\/sysbio\/syq085","volume":"60","author":"W Xie","year":"2011","unstructured":"Xie, W., Lewis, P. O., Fan, Y., Kuo, L. & Chen, M. H. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst. Biol. \n                           60, 150\u2013160 (2011).","journal-title":"Syst. Biol."},{"key":"1449_CR50","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1534\/genetics.116.190496","volume":"204","author":"MA Ansari","year":"2016","unstructured":"Ansari, M. A. & Didelot, X. Bayesian inference of the evolution of a phenotype distribution on a phylogenetic tree. Genetics \n                           204, 89\u201398 (2016).","journal-title":"Genetics"},{"key":"1449_CR51","doi-asserted-by":"publisher","first-page":"1536","DOI":"10.1093\/bioinformatics\/bts184","volume":"28","author":"AA Popescu","year":"2012","unstructured":"Popescu, A. A., Huber, K. T. & Paradis, E. ape 3.0: new tools for distance-based phylogenetics and evolutionary analysis in R. Bioinformatics \n                           28, 1536\u20131537 (2012).","journal-title":"Bioinformatics"},{"key":"1449_CR52","unstructured":"R Development Core Team. R: a language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria, 2008)."},{"key":"1449_CR53","volume":"2","author":"S Argim\u00f3n","year":"2016","unstructured":"Argim\u00f3n, S. et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb. Genome \n                           2, 11 (2016).","journal-title":"Microb. Genome"},{"key":"1449_CR54","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1111\/2041-210X.12466","volume":"7","author":"GGR Murray","year":"2016","unstructured":"Murray, G. G. R. et al. The effect of genetic structure on molecular dating and tests for temporal signal. Methods Ecol. Evol. \n                           7, 80\u201389 (2016).","journal-title":"Methods Ecol. Evol."},{"key":"1449_CR55","doi-asserted-by":"publisher","first-page":"1403","DOI":"10.1093\/bioinformatics\/btn129","volume":"24","author":"T Jombart","year":"2008","unstructured":"Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics \n                           24, 1403\u20131405 (2008).","journal-title":"Bioinformatics"},{"key":"1449_CR56","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-10-421","volume":"10","author":"C Camacho","year":"2009","unstructured":"Camacho, C. et al. Blast+: architecture and applications. BMC Bioinformatics \n                           10, 1 (2009).","journal-title":"BMC Bioinformatics"},{"key":"1449_CR57","doi-asserted-by":"publisher","first-page":"D325","DOI":"10.1093\/nar\/gki008","volume":"33","author":"L Cheng","year":"2005","unstructured":"Cheng, L. et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. \n                           33, D325\u2013D328 (2005).","journal-title":"Nucleic Acids Res."},{"key":"1449_CR58","doi-asserted-by":"publisher","first-page":"D581","DOI":"10.1093\/nar\/gkt1099","volume":"42","author":"AR Wattam","year":"2014","unstructured":"Wattam, A. R. et al. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. \n                           42, D581\u2013D591 (2014).","journal-title":"Nucleic Acids Res."},{"key":"1449_CR59","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1002195","volume":"7","author":"SR Eddy","year":"2011","unstructured":"Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. \n                           7, e1002195 (2011).","journal-title":"PLoS Comput. Biol."},{"key":"1449_CR60","doi-asserted-by":"publisher","first-page":"D138","DOI":"10.1093\/nar\/gkh121","volume":"32","author":"A Bateman","year":"2004","unstructured":"Bateman, A. et al. The Pfam protein families database. Nucleic Acids Res. \n                           32, D138\u2013D141 (2004).","journal-title":"Nucleic Acids Res."},{"key":"1449_CR61","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-016-2627-0","volume":"17","author":"A Biswas","year":"2016","unstructured":"Biswas, A., Staals, R. H. J., Morales, S. E., Fineran, P. C. & Brown, C. M. CRISPRDetect: a flexible algorithm to define CRISPR arrays. BMC Genomics \n                           17, 356 (2016).","journal-title":"BMC Genomics"},{"key":"1449_CR62","doi-asserted-by":"publisher","first-page":"1719","DOI":"10.1038\/ismej.2017.36","volume":"11","author":"NA Andreani","year":"2017","unstructured":"Andreani, N. A., Hesse, E. & Vos, M. Prokaryote genome fluidity is dependent on effective population size. ISME J. \n                           11, 1719\u20131721 (2017).","journal-title":"ISME J."},{"key":"1449_CR63","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-12-32","volume":"12","author":"AO Kislyuk","year":"2011","unstructured":"Kislyuk, A. O., Haegeman, B., Bergman, N. H. & Weitz, J. S. Genomic fluidity: an integrative view of gene diversity within microbial populations. BMC Genomics \n                           12, 32 (2011).","journal-title":"BMC Genomics"},{"key":"1449_CR64","doi-asserted-by":"publisher","first-page":"592","DOI":"10.1093\/bioinformatics\/btq706","volume":"27","author":"KP Schliep","year":"2010","unstructured":"Schliep, K. P. phangorn: phylogenetic analysis in R. Bioinformatics \n                           27, 592\u2013593 (2010).","journal-title":"Bioinformatics"},{"key":"1449_CR65","doi-asserted-by":"publisher","first-page":"2073","DOI":"10.1093\/bioinformatics\/btu154","volume":"30","author":"Z Li","year":"2014","unstructured":"Li, Z. et al. CorMut: an R\/Bioconductor package for computing correlated mutations based on selection pressure. Bioinformatics \n                           30, 2073\u20132075 (2014).","journal-title":"Bioinformatics"}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-01449-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-01449-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-01449-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,22]],"date-time":"2022-12-22T22:19:09Z","timestamp":1671747549000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-01449-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,11,8]]},"references-count":65,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["1449"],"URL":"https:\/\/doi.org\/10.1038\/s41467-017-01449-9","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,11,8]]},"assertion":[{"value":"13 February 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 September 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 November 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"1367"}}