{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,19]],"date-time":"2025-12-19T09:33:06Z","timestamp":1766136786225,"version":"3.37.3"},"reference-count":64,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2016,11,3]],"date-time":"2016-11-03T00:00:00Z","timestamp":1478131200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["260421-ECOADAPT"],"award-info":[{"award-number":["260421-ECOADAPT"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["PTDC\/BIA-EVF\/118075\/2010"],"award-info":[{"award-number":["PTDC\/BIA-EVF\/118075\/2010"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BD\/80257\/2011"],"award-info":[{"award-number":["SFRH\/BD\/80257\/2011"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BPD\/111725\/2015"],"award-info":[{"award-number":["SFRH\/BPD\/111725\/2015"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["RECI\/IMI-IMU\/0038\/2012"],"award-info":[{"award-number":["RECI\/IMI-IMU\/0038\/2012"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["SFB 680"],"award-info":[{"award-number":["SFB 680"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"DOI":"10.1371\/journal.pgen.1006420","type":"journal-article","created":{"date-parts":[[2016,11,3]],"date-time":"2016-11-03T17:52:44Z","timestamp":1478195564000},"page":"e1006420","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":46,"title":["A Mutational Hotspot and Strong Selection Contribute to the Order of Mutations Selected for during Escherichia coli Adaptation to the Gut"],"prefix":"10.1371","volume":"12","author":[{"given":"Marta","family":"Louren\u00e7o","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4834-6997","authenticated-orcid":true,"given":"Ricardo S.","family":"Ramiro","sequence":"additional","affiliation":[]},{"given":"Daniela","family":"G\u00fcleresi","sequence":"additional","affiliation":[]},{"given":"Jo\u00e3o","family":"Barroso-Batista","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5210-1434","authenticated-orcid":true,"given":"Karina B.","family":"Xavier","sequence":"additional","affiliation":[]},{"given":"Isabel","family":"Gordo","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7276-4195","authenticated-orcid":true,"given":"Ana","family":"Sousa","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2016,11,3]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1038\/nature11550","article-title":"Diversity, stability and resilience of the human gut microbiota","volume":"489","author":"CA Lozupone","year":"2012","journal-title":"Nature"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1016\/j.immuni.2014.05.012","article-title":"Mining the Human Gut Microbiota for Effector Strains that Shape the Immune System","volume":"40","author":"PP Ahern","year":"2014","journal-title":"Immunity"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.cell.2014.12.038","article-title":"Extensive Strain-Level Copy-Number Variation across Human Gut Microbiome Species","volume":"160","author":"S Greenblum","year":"2015","journal-title":"Cell"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"e1002050","DOI":"10.1371\/journal.pbio.1002050","article-title":"Where Next for Microbiome Research?","volume":"13","author":"MK Waldor","year":"2015","journal-title":"PLOS Biol"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1098\/rstb.1988.0059","article-title":"Frequency-dependent selection in bacterial populations","volume":"319","author":"BR Levin","year":"1988","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"e1000627","DOI":"10.1371\/journal.pgen.1000627","article-title":"Toward the Use of Genomics to Study Microevolutionary Change in Bacteria","volume":"5","author":"D Falush","year":"2009","journal-title":"PLoS Genet"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1038\/nrg2146","article-title":"The distribution of fitness effects of new mutations","volume":"8","author":"A Eyre-Walker","year":"2007","journal-title":"Nat Rev Genet"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"e1004182","DOI":"10.1371\/journal.pgen.1004182","article-title":"The First Steps of Adaptation of Escherichia coli to the Gut Are Dominated by Soft Sweeps","volume":"10","author":"J Barroso-Batista","year":"2014","journal-title":"PLoS Genet"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"1615","DOI":"10.1126\/science.1122469","article-title":"An Equivalence Principle for the Incorporation of Favorable Mutations in Asexual Populations","volume":"311","author":"M Hegreness","year":"2006","journal-title":"Science"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1038\/nrg3937","article-title":"Elucidating the molecular architecture of adaptation via evolve and resequence experiments","volume":"16","author":"A Long","year":"2015","journal-title":"Nat Rev Genet"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1111\/j.1432-1033.1994.tb18903.x","article-title":"Transport of C4-dicarboxylates by anaerobically grown Escherichia coli. Energetics and mechanism of exchange, uptake and efflux","volume":"222","author":"P Engel","year":"1994","journal-title":"Eur J Biochem FEBS"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1111\/j.1365-2958.1994.tb00375.x","article-title":"Isolation and characterization of hypophosphite\u2014resistant mutants of Escherichia coli: identification of the FocA protein, encoded by the pfl operon, as a putative formate transporter","volume":"11","author":"B Suppmann","year":"1994","journal-title":"Mol Microbiol"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"4891","DOI":"10.1128\/IAI.00484-07","article-title":"Respiration of Escherichia coli in the Mouse Intestine","volume":"75","author":"SA Jones","year":"2007","journal-title":"Infect Immun"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"4218","DOI":"10.1128\/IAI.05395-11","article-title":"Anaerobic Respiration of Escherichia coli in the Mouse Intestine","volume":"79","author":"SA Jones","year":"2011","journal-title":"Infect Immun"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"926","DOI":"10.1128\/JB.01447-07","article-title":"Regulation of the yjjQ-bglJ Operon, Encoding LuxR-Type Transcription Factors, and the Divergent yjjP Gene by H-NS and LeuO","volume":"190","author":"T Stratmann","year":"2008","journal-title":"J Bacteriol"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1128\/jb.165.2.434-442.1986","article-title":"opp-lac Operon fusions and transcriptional regulation of the Escherichia coli trp-linked oligopeptide permease","volume":"165","author":"JC Andrews","year":"1986","journal-title":"J Bacteriol"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"20130838","DOI":"10.1098\/rsbl.2013.0838","article-title":"Rates of transposition in Escherichia coli","volume":"9","author":"A Sousa","year":"2013","journal-title":"Biol Lett"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nrg3095","article-title":"Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence","volume":"13","author":"PJ Wittkopp","year":"2012","journal-title":"Nat Rev Genet"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT-PCR","volume":"29","author":"MW Pfaffl","year":"2001","journal-title":"Nucleic Acids Res"},{"key":"ref20","first-page":"269","article-title":"The molecular biology of formate metabolism in enterobacteria","volume":"4","author":"S Leonhartsberger","year":"2002","journal-title":"J Mol Microbiol Biotechnol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"e1003839","DOI":"10.1371\/journal.pgen.1003839","article-title":"The Bacterial Response Regulator ArcA Uses a Diverse Binding Site Architecture to Regulate Carbon Oxidation Globally","volume":"9","author":"DM Park","year":"2013","journal-title":"PLoS Genet"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"7427","DOI":"10.1073\/pnas.0307888101","article-title":"Carbon nutrition of Escherichia coli in the mouse intestine","volume":"101","author":"D-E Chang","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1038\/ng1535","article-title":"An empirical test of the mutational landscape model of adaptation using a single-stranded DNA virus","volume":"37","author":"DR Rokyta","year":"2005","journal-title":"Nat Genet"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1038\/nrg3744","article-title":"Empirical fitness landscapes and the predictability of evolution","volume":"15","author":"JAGM de Visser","year":"2014","journal-title":"Nat Rev Genet"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"1564","DOI":"10.1093\/bioinformatics\/btp253","article-title":"Fluctuation AnaLysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis","volume":"25","author":"BM Hall","year":"2009","journal-title":"Bioinformatics"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"e1003617","DOI":"10.1371\/journal.pgen.1003617","article-title":"Bacterial Adaptation through Loss of Function","volume":"9","author":"AK Hottes","year":"2013","journal-title":"PLoS Genet"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"8945","DOI":"10.1038\/ncomms9945","article-title":"Adaptive immunity increases the pace and predictability of evolutionary change in commensal gut bacteria","volume":"6","author":"J Barroso-Batista","year":"2015","journal-title":"Nat Commun"},{"key":"ref28","first-page":"1165","article-title":"Perspective: Sign epistasis and genetic constraint on evolutionary trajectories","volume":"59","author":"DM Weinreich","year":"2005","journal-title":"Evol Int J Org Evol"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1126\/science.1203801","article-title":"Negative epistasis between beneficial mutations in an evolving bacterial population","volume":"332","author":"AI Khan","year":"2011","journal-title":"Science"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1126\/science.1203799","article-title":"Diminishing returns epistasis among beneficial mutations decelerates adaptation","volume":"332","author":"H-H Chou","year":"2011","journal-title":"Science"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"e1002075","DOI":"10.1371\/journal.pgen.1002075","article-title":"Epistasis between beneficial mutations and the phenotype-to-fitness Map for a ssDNA virus","volume":"7","author":"DR Rokyta","year":"2011","journal-title":"PLoS Genet"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1534\/genetics.110.121400","article-title":"Mutational Effects and Population Dynamics During Viral Adaptation Challenge Current Models","volume":"187","author":"CR Miller","year":"2011","journal-title":"Genetics"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"e1000250","DOI":"10.1371\/journal.pbio.1000250","article-title":"The properties of adaptive walks in evolving populations of fungus","volume":"7","author":"SE Schoustra","year":"2009","journal-title":"PLoS Biol"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"99","DOI":"10.3389\/fgene.2015.00099","article-title":"The rule of declining adaptability in microbial evolution experiments","volume":"6","author":"A Couce","year":"2015","journal-title":"Front Genet"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1534\/genetics.109.106195","article-title":"The genetic basis of phenotypic adaptation II: the distribution of adaptive substitutions in the moving optimum model","volume":"183","author":"M Kopp","year":"2009","journal-title":"Genetics"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"20120239","DOI":"10.1098\/rsbl.2012.0239","article-title":"Evolution of clonal populations approaching a fitness peak","volume":"9","author":"I Gordo","year":"2012","journal-title":"Biol Lett"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.tig.2009.01.002","article-title":"From fitness landscapes to seascapes: non-equilibrium dynamics of selection and adaptation","volume":"25","author":"V Mustonen","year":"2009","journal-title":"Trends Genet TIG"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1002\/bies.201500151","article-title":"Know your neighbor: Microbiota and host epithelial cells interact locally to control intestinal function and physiology","volume":"38","author":"F Sommer","year":"2016","journal-title":"BioEssays"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1038\/npp.2014.224","article-title":"More than a Gut Feeling: the Microbiota Regulates Neurodevelopment and Behavior","volume":"40","author":"JF Cryan","year":"2015","journal-title":"Neuropsychopharmacology"},{"key":"ref40","first-page":"75","article-title":"Polymorphism in Escherichia coli: rtl atl and gat regions behave as chromosomal alternatives","volume":"129","author":"MJ Woodward","year":"1983","journal-title":"J Gen Microbiol"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"760","DOI":"10.1111\/evo.12301","article-title":"Sign epistasis limits evolutionary trade-offs at the confluence of single- and multi-carbon metabolism in Methylobacterium extorquens AM1","volume":"68","author":"SM Carroll","year":"2014","journal-title":"Evol Int J Org Evol"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"n\/a","DOI":"10.1111\/1574-6976.12082","article-title":"The functional basis of adaptive evolution in chemostats","author":"D Gresham","year":"2014","journal-title":"FEMS Microbiol Rev"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/0006-3002(62)90941-1","article-title":"Isolation and properties of bacteria capable of high rates of beta-galactosidase synthesis","volume":"55","author":"T Horiuchi","year":"1962","journal-title":"Biochim Biophys Acta"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1093\/oxfordjournals.molbev.a026009","article-title":"Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment","volume":"15","author":"CJ Brown","year":"1998","journal-title":"Mol Biol Evol"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1093\/gbe\/evv004","article-title":"Simple phenotypic sweeps hide complex genetic changes in populations","volume":"7","author":"RP Maharjan","year":"2015","journal-title":"Genome Biol Evol"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"R41","DOI":"10.1186\/gb-2012-13-6-r41","article-title":"The multiplicity of divergence mechanisms in a single evolving population","volume":"13","author":"RP Maharjan","year":"2012","journal-title":"Genome Biol"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.gde.2015.08.008","article-title":"Genomic investigations of evolutionary dynamics and epistasis in microbial evolution experiments","volume":"35","author":"ER Jerison","year":"2015","journal-title":"Curr Opin Genet Dev"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"3617","DOI":"10.1098\/rspb.2011.1537","article-title":"The causes of epistasis","volume":"278","author":"JAGM de Visser","year":"2011","journal-title":"Proc R Soc B Biol Sci"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1126\/science.1248688","article-title":"Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli","volume":"343","author":"J Plucain","year":"2014","journal-title":"Science"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"e1004149","DOI":"10.1371\/journal.pgen.1004149","article-title":"Mapping the Fitness Landscape of Gene Expression Uncovers the Cause of Antagonism and Sign Epistasis between Adaptive Mutations","volume":"10","author":"H-H Chou","year":"2014","journal-title":"PLoS Genet"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"e1005404","DOI":"10.1371\/journal.pgen.1005404","article-title":"Coordinated Evolution of Influenza A Surface Proteins","volume":"11","author":"AD Neverov","year":"2015","journal-title":"PLOS Genet"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"2834","DOI":"10.1128\/JB.183.9.2834-2841.2001","article-title":"Mechanisms Causing Rapid and Parallel Losses of Ribose Catabolism in Evolving Populations of Escherichia coli B","volume":"183","author":"VS Cooper","year":"2001","journal-title":"J Bacteriol"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1126\/science.277.5331.1453","article-title":"The complete genome sequence of Escherichia coli K-12","volume":"277","author":"FR Blattner","year":"1997","journal-title":"Science"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"2006","DOI":"10.1038\/msb4100050","article-title":"Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection","volume":"2","author":"T Baba","year":"2006","journal-title":"Mol Syst Biol"},{"key":"ref55","article-title":"The Life of Commensal Escherichia coli in the Mammalian Intestine","volume":"1","author":"KA Krogfelt","year":"2013","journal-title":"EcoSal Plus"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"5840","DOI":"10.1128\/jb.177.20.5840-5845.1995","article-title":"Physiological state of Escherichia coli BJ4 growing in the large intestines of streptomycin-treated mice","volume":"177","author":"LK Poulsen","year":"1995","journal-title":"J Bacteriol"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1128\/CDLI.6.3.434-436.1999","article-title":"Estimation of growth rates of Escherichia coli BJ4 in streptomycin-treated and previously germfree mice by in situ rRNA hybridization","volume":"6","author":"CU Rang","year":"1999","journal-title":"Clin Diagn Lab Immunol"},{"key":"ref58","first-page":"2.4.1","article-title":"Current Protocols in Molecular Biology","author":"K Wilson","year":"2001"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1038\/nature08480","article-title":"Genome evolution and adaptation in a long-term experiment with Escherichia coli","volume":"461","author":"JE Barrick","year":"2009","journal-title":"Nature"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"1725","DOI":"10.1101\/gr.194201","article-title":"SSAHA: a fast search method for large DNA databases","volume":"11","author":"Z Ning","year":"2001","journal-title":"Genome Res"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nbt.1754","article-title":"Integrative genomics viewer","volume":"29","author":"JT Robinson","year":"2011","journal-title":"Nat Biotechnol"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1128\/JB.132.1.166-173.1977","article-title":"Xylitol and D-arabitol toxicities due to derepressed fructose, galactitol, and sorbitol phosphotransferases of Escherichia coli","volume":"132","author":"AM Reiner","year":"1977","journal-title":"J Bacteriol"},{"year":"2016","key":"ref63","article-title":"R: A language and environment for statistical computing [Internet]"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"D583","DOI":"10.1093\/nar\/gkq1143","article-title":"EcoCyc: a comprehensive database of Escherichia coli biology","volume":"39","author":"IM Keseler","year":"2011","journal-title":"Nucleic Acids Res"}],"container-title":["PLOS Genetics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pgen.1006420","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,9,27]],"date-time":"2020-09-27T03:38:26Z","timestamp":1601177906000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1006420"}},"subtitle":[],"editor":[{"given":"Tim F","family":"Cooper","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2016,11,3]]},"references-count":64,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2016,11,3]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1006420","relation":{},"ISSN":["1553-7404"],"issn-type":[{"type":"electronic","value":"1553-7404"}],"subject":[],"published":{"date-parts":[[2016,11,3]]}}}