{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,11]],"date-time":"2026-03-11T23:27:18Z","timestamp":1773271638800,"version":"3.50.1"},"reference-count":22,"publisher":"Oxford University Press (OUP)","issue":"13","license":[{"start":{"date-parts":[[2016,10,2]],"date-time":"2016-10-02T00:00:00Z","timestamp":1475366400000},"content-version":"vor","delay-in-days":3015,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/2.0\/uk\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2008,7,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Motivation: In bacterial evolution, inferring a strain tree, which is the evolutionary history of different strains of the same bacterium, plays a major role in analyzing and understanding the evolution of strongly isolated populations, population divergence and various evolutionary events, such as horizontal gene transfer and homologous recombination. Inferring a strain tree from multilocus data of these strains is exceptionally hard since, at this scale of evolution, processes such as homologous recombination result in a very high degree of gene tree incongruence.<\/jats:p><jats:p>Results: In this article we present a novel computational method for inferring the strain tree despite massive gene tree incongruence caused by homologous recombination. Our method operates in three phases, where in phase I a set of candidate strain-tree topologies is computed using the maximal cliques concept, in phase II divergence times for each of the topologies are estimated using mixed integer linear programming (MILP) and in phase III the optimal tree (or trees) is selected based on an optimality criterion. We have analyzed 1898 genes from nine strains of the Staphylococcus aureus bacteria, and identified a fully resolved (binary) strain tree with estimated divergence times, despite the high degrees of sequence identity at the nucleotide level and gene tree incongruence. Our method's efficiency makes it particularly suitable for analysis of genome-scale datasets, including those of strongly isolated populations which are usually very challenging to analyze.<\/jats:p><jats:p>Availability: We have implemented the algorithms in the PhyloNet software package, which is available publicly at http:\/\/bioinfo.cs.rice.edu\/phylonet\/<\/jats:p><jats:p>Contact: \u00a0nakhleh@cs.rice.edu<\/jats:p>","DOI":"10.1093\/bioinformatics\/btn149","type":"journal-article","created":{"date-parts":[[2008,6,27]],"date-time":"2008-06-27T07:43:13Z","timestamp":1214552593000},"page":"i123-i131","source":"Crossref","is-referenced-by-count":18,"title":["Efficient inference of bacterial strain trees from genome-scale multilocus data"],"prefix":"10.1093","volume":"24","author":[{"given":"C.","family":"Than","sequence":"first","affiliation":[{"name":"1 Department of Computer Science, Rice University, Houston, TX 77005, USA and 2Department of Evolutionary Studies of Biosystems, Graduate University for Advanced Studies, School of Advanced Sciences, Hayama, Kanagawa 240-0193, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"R.","family":"Sugino","sequence":"additional","affiliation":[{"name":"1 Department of Computer Science, Rice University, Houston, TX 77005, USA and 2Department of Evolutionary Studies of Biosystems, Graduate University for Advanced Studies, School of Advanced Sciences, Hayama, Kanagawa 240-0193, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"H.","family":"Innan","sequence":"additional","affiliation":[{"name":"1 Department of Computer Science, Rice University, Houston, TX 77005, USA and 2Department of Evolutionary Studies of Biosystems, Graduate University for Advanced Studies, School of Advanced Sciences, Hayama, Kanagawa 240-0193, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"L.","family":"Nakhleh","sequence":"additional","affiliation":[{"name":"1 Department of Computer Science, Rice University, Houston, TX 77005, USA and 2Department of Evolutionary Studies of Biosystems, Graduate University for Advanced Studies, School of Advanced Sciences, Hayama, Kanagawa 240-0193, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2008,7,1]]},"reference":[{"key":"2023020210361900600_B1","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped BLAST and PSI-BLAST: a new generation of protein database search programs","volume":"25","author":"Altschul","year":"1997","journal-title":"Nucleic Acids Res"},{"key":"2023020210361900600_B2","doi-asserted-by":"crossref","first-page":"1819","DOI":"10.1016\/S0140-6736(02)08713-5","article-title":"Genome and virulence determinants of high virulence community-acquired MRSA","volume":"359","author":"Baba","year":"2002","journal-title":"Lancet"},{"key":"2023020210361900600_B3","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1371\/journal.pgen.0020068","article-title":"Discordance of species trees with their most likely gene trees","volume":"2","author":"Degnan","year":"2006","journal-title":"PLoS Genetics"},{"key":"2023020210361900600_B4","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1016\/S0140-6736(06)68231-7","article-title":"Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus","volume":"367","author":"Diep","year":"2006","journal-title":"Lancet"},{"key":"2023020210361900600_B5","doi-asserted-by":"crossref","first-page":"5936","DOI":"10.1073\/pnas.0607004104","article-title":"High-resolution species trees without concatenation","volume":"104","author":"Edwards","year":"2007","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023020210361900600_B6","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1038\/35080005","article-title":"DNA transport in bacteria","volume":"2","author":"Errington","year":"2001","journal-title":"Nat. Rev. Mol. Cell Biol"},{"key":"2023020210361900600_B7","doi-asserted-by":"crossref","first-page":"2426","DOI":"10.1128\/JB.187.7.2426-2438.2005","article-title":"Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain","volume":"187","author":"Gill","year":"2005","journal-title":"J.n Bacteriol"},{"key":"2023020210361900600_B8","doi-asserted-by":"crossref","first-page":"e1120","DOI":"10.1371\/journal.pone.0001120","article-title":"Molecular correlates of host specialization in staphylococcus aureus","volume":"2","author":"Herron-Olson","year":"2007","journal-title":"PLoS ONE"},{"key":"2023020210361900600_B9","doi-asserted-by":"crossref","first-page":"9786","DOI":"10.1073\/pnas.0402521101","article-title":"Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance","volume":"101","author":"Holden","year":"2004","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023020210361900600_B10","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1080\/10635150601146041","article-title":"Inconsistency of phylogenetic estimates from concatenated data under coalescence","volume":"56","author":"Kubatko","year":"2007","journal-title":"Syst. Biol"},{"key":"2023020210361900600_B11","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.1016\/S0140-6736(00)04403-2","article-title":"Whole genome sequencing of meticillin-resistant Staphylococcus aureus","volume":"357","author":"Kuroda","year":"2001","journal-title":"Lancet"},{"key":"2023020210361900600_B12","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1080\/10635150500354928","article-title":"Inferring phylogeny despite incomplete lineage sorting","volume":"55","author":"Maddison","year":"2006","journal-title":"Syst. Biol"},{"key":"2023020210361900600_B13","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1093\/genetics\/120.2.359","article-title":"Molecular evolution of the Eschericia coli chromosome. II. Clonal segments","volume":"120","author":"Milkman","year":"1988","journal-title":"Genetics"},{"key":"2023020210361900600_B14","doi-asserted-by":"crossref","DOI":"10.1093\/oso\/9780195135848.001.0001","volume-title":"Molecular Evolution and Phylogenetics","author":"Nei","year":"2000"},{"key":"2023020210361900600_B15","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1007\/BF02111283","article-title":"Evolution in bacteria: evidence for a universal substitution rate in cellular genomes","volume":"26","author":"Ochman","year":"1987","journal-title":"J. Mol. Evol"},{"key":"2023020210361900600_B16","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1126\/science.1144876","article-title":"Temporal fragmentation of speciation in bacteria","volume":"317","author":"Retchless","year":"2007","journal-title":"Science"},{"key":"2023020210361900600_B17","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/0025-5564(81)90043-2","article-title":"Comparison of phylogenetic trees","volume":"53","author":"Robinson","year":"1981","journal-title":"Math. Biosciences"},{"key":"2023020210361900600_B18","doi-asserted-by":"crossref","first-page":"798","DOI":"10.1038\/nature02053","article-title":"Genome-scale approaches to resolving incongruence in molecular phylogenies","volume":"425","author":"Rokas","year":"2003","journal-title":"Nature"},{"key":"2023020210361900600_B19","first-page":"406","article-title":"The neighbor-joining method: a new method for reconstructing phylogenetic trees","volume":"4","author":"Saitou","year":"1987","journal-title":"Mol. Biol. Evol"},{"key":"2023020210361900600_B20","doi-asserted-by":"crossref","DOI":"10.1093\/oso\/9780198509424.001.0001","volume-title":"Phylogenetics","author":"Semple","year":"2003"},{"key":"2023020210361900600_B21","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1093\/genetics\/120.2.345","article-title":"Molecular evolution of the Escherichia coli chromosome. I. Analysis of structure and natural variation in a previously uncharacterized region between trp and tonB","volume":"120","author":"Stoltzfus","year":"1988","journal-title":"Genetics"},{"key":"2023020210361900600_B22","volume-title":"PAUP*: Phylogenetic Analysis using Parsimony","author":"Swofford","year":"2003"}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/24\/13\/i123\/49051837\/bioinformatics_24_13_i123.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/24\/13\/i123\/49051837\/bioinformatics_24_13_i123.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,27]],"date-time":"2024-02-27T22:21:21Z","timestamp":1709072481000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/24\/13\/i123\/228890"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2008,7,1]]},"references-count":22,"journal-issue":{"issue":"13","published-print":{"date-parts":[[2008,7,1]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btn149","relation":{},"ISSN":["1367-4811","1367-4803"],"issn-type":[{"value":"1367-4811","type":"electronic"},{"value":"1367-4803","type":"print"}],"subject":[],"published-other":{"date-parts":[[2008,7,1]]},"published":{"date-parts":[[2008,7,1]]}}}