{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T14:40:06Z","timestamp":1791384006794,"version":"4.3.3"},"reference-count":93,"publisher":"American Society for Microbiology","issue":"2","license":[{"start":{"date-parts":[[2019,3,5]],"date-time":"2019-03-05T00:00:00Z","timestamp":1551744000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,4,30]],"date-time":"2019-04-30T00:00:00Z","timestamp":1556582400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"DOI":"10.13039\/100000002","name":"HHS | National Institutes of Health","doi-asserted-by":"publisher","award":["AI39557"],"award-info":[{"award-number":["AI39557"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"HHS | National Institutes of Health","doi-asserted-by":"publisher","award":["AI44486"],"award-info":[{"award-number":["AI44486"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"HHS | National Institutes of Health","doi-asserted-by":"publisher","award":["AI118962"],"award-info":[{"award-number":["AI118962"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"HHS | National Institutes of Health","doi-asserted-by":"publisher","award":["AI112640"],"award-info":[{"award-number":["AI112640"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"HHS | National Institutes of Health","doi-asserted-by":"publisher","award":["A148622"],"award-info":[{"award-number":["A148622"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["mBio"],"published-print":{"date-parts":[[2019,4,30]]},"abstract":"<jats:p>\n                    Bacteria primarily evolve via horizontal gene transfer, acquiring new traits such as virulence and antibiotic resistance in single transfer events. However, newly acquired genes must be integrated into existing regulatory networks to allow appropriate expression in new hosts. This is accommodated in part by the opposing mechanisms of xenogeneic silencing and countersilencing. An understanding of these mechanisms is necessary to understand the relationship between gene regulation and bacterial evolution. Here we examine the functional evolution of an important lineage of countersilencers belonging to the ancient MarR family of classical transcriptional repressors. We show that although members of the SlyA lineage retain some ancestral features associated with the MarR family, their\n                    <jats:italic>cis<\/jats:italic>\n                    -regulatory sequences have evolved significantly to support their new function. Understanding the mechanistic requirements for countersilencing is critical to understanding the pathoadaptation of emerging pathogens and also has practical applications in synthetic biology.\n                  <\/jats:p>","DOI":"10.1128\/mbio.00009-19","type":"journal-article","created":{"date-parts":[[2019,3,4]],"date-time":"2019-03-04T05:36:13Z","timestamp":1551677773000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":30,"title":["The Evolution of SlyA\/RovA Transcription Factors from Repressors to Countersilencers in\n                    <i>Enterobacteriaceae<\/i>"],"prefix":"10.1128","volume":"10","author":[{"given":"W. Ryan","family":"Will","sequence":"first","affiliation":[{"name":"Department of Laboratory Medicine, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Brzovic","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isolde","family":"Le Trong","sequence":"additional","affiliation":[{"name":"Department of Biological Structure, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ronald E.","family":"Stenkamp","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, University of Washington, Seattle, Washington, USA"},{"name":"Department of Biological Structure, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew B.","family":"Lawrenz","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology and the Center for Predictive Medicine for Biodefense and Emerging Infectious Diseases, University of Louisville School of Medicine, Louisville, Kentucky, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joyce E.","family":"Karlinsey","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William W.","family":"Navarre","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kara","family":"Main-Hester","sequence":"additional","affiliation":[{"name":"Department of Microbiology, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Virginia L.","family":"Miller","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of North Carolina School of Medicine, Chapel Hill, North Carolina, USA"},{"name":"Department of Genetics, University of North Carolina School of Medicine, Chapel Hill, North Carolina, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen J.","family":"Libby","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3243-110X","authenticated-orcid":false,"given":"Ferric C.","family":"Fang","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, University of Washington, Seattle, Washington, USA"},{"name":"Department of Microbiology, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2016.07.010"},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-642-86659-3"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1038\/378140a0"},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.25.14658"},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1038\/ng1340"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.compbiolchem.2004.09.004"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.csbj.2017.06.001"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1038\/90429"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.177.12.3414-3419.1995"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.92.12.5456"},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.155.2.531-540.1983"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.175.24.7856-7862.1993"},{"key":"e_1_3_2_14_2","first-page":"51","article-title":"Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins","volume":"8","author":"Wilkinson SP","year":"2006","unstructured":"Wilkinson SP, Grove A. 2006. Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins. Curr Issues Mol Biol 8:51\u201362.","journal-title":"Curr Issues Mol Biol"},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0966-842X(99)01589-9"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1038\/nchembio.1380"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00775-017-1442-7"},{"key":"e_1_3_2_18_2","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms6270"},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.mib.2014.10.005"},{"key":"e_1_3_2_20_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2007.05950.x"},{"key":"e_1_3_2_21_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M709843200"},{"key":"e_1_3_2_22_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2005.04553.x"},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0092-8674(00)81003-X"},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2007.03.008"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2005.05.030"},{"key":"e_1_3_2_26_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1997.5981976.x"},{"key":"e_1_3_2_27_2","doi-asserted-by":"publisher","DOI":"10.1099\/00207713-49-1-267"},{"key":"e_1_3_2_28_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.15.4517-4525.2001"},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0603456103"},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2007.05907.x"},{"key":"e_1_3_2_31_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2004.04162.x"},{"key":"e_1_3_2_32_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00240-09"},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.00806-15"},{"key":"e_1_3_2_34_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M111.245258"},{"key":"e_1_3_2_35_2","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.000423"},{"key":"e_1_3_2_36_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkv1156"},{"key":"e_1_3_2_37_2","doi-asserted-by":"publisher","DOI":"10.1093\/jmcb\/mjq021"},{"key":"e_1_3_2_38_2","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1007\/978-3-642-38922-1_167","volume-title":"The prokaryotes: gammaproteobacteria.","author":"Octavia S","year":"2014","unstructured":"Octavia S, Lan R. 2014. The family Enterobacteriaceae, p 225\u2013286. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (ed), The prokaryotes: gammaproteobacteria. Springer, Berlin, Germany."},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.89.19.8938"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.177.9.2328-2334.1995"},{"key":"e_1_3_2_41_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00862-05"},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.2000.01740.x"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M504464200"},{"key":"e_1_3_2_44_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.176.21.6769-6775.1994"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1002\/j.1460-2075.1996.tb00877.x"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2004.04421.x"},{"key":"e_1_3_2_47_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M111.266619"},{"key":"e_1_3_2_48_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.186.6.1620-1628.2004"},{"key":"e_1_3_2_49_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M703465200"},{"key":"e_1_3_2_50_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2008.01.001"},{"key":"e_1_3_2_51_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2005.09.013"},{"key":"e_1_3_2_52_2","doi-asserted-by":"publisher","DOI":"10.1038\/ismej.2017.18"},{"key":"e_1_3_2_53_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.07021-11"},{"key":"e_1_3_2_54_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.py.30.090192.002101"},{"key":"e_1_3_2_55_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gks1201"},{"key":"e_1_3_2_56_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2013.11.010"},{"key":"e_1_3_2_57_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00528-07"},{"key":"e_1_3_2_58_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.02096-14"},{"key":"e_1_3_2_59_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0811669106"},{"key":"e_1_3_2_60_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.37.2.506-512.1982"},{"key":"e_1_3_2_61_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M112.379156"},{"key":"e_1_3_2_62_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.120163297"},{"key":"e_1_3_2_63_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0044841"},{"key":"e_1_3_2_64_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.65.4.1610-1618.1999"},{"key":"e_1_3_2_65_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.175.21.6902-6907.1993"},{"key":"e_1_3_2_66_2","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.00143-12"},{"key":"e_1_3_2_67_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0404012101"},{"key":"e_1_3_2_68_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.65.6.2497-2501.1997"},{"key":"e_1_3_2_69_2","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1119(91)90366-J"},{"key":"e_1_3_2_70_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.177.14.4121-4130.1995"},{"key":"e_1_3_2_71_2","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1119(88)90440-4"},{"key":"e_1_3_2_72_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1119(99)00434-5"},{"key":"e_1_3_2_73_2","doi-asserted-by":"publisher","DOI":"10.1002\/0471142727.mb2103s69"},{"key":"e_1_3_2_74_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.01206-08"},{"key":"e_1_3_2_75_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.05877-11"},{"key":"e_1_3_2_76_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00197809"},{"key":"e_1_3_2_77_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00404272"},{"key":"e_1_3_2_78_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0076-6879(97)76066-X"},{"key":"e_1_3_2_79_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0021889897006766"},{"key":"e_1_3_2_80_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkg520"},{"key":"e_1_3_2_81_2","doi-asserted-by":"crossref","unstructured":"Lunin V Evdokimova E Kudritska M Osipiuk J Joachimiak A Edwards A Savchenko A Midwest Center for Structural Genomics. 2005. The crystal structure of transcriptional regulator PA3341. RCSB PDB accession no. 2FBH.","DOI":"10.2210\/pdb2fbh\/pdb"},{"key":"e_1_3_2_82_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444996012255"},{"key":"e_1_3_2_83_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444994003112"},{"key":"e_1_3_2_84_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444992007352"},{"key":"e_1_3_2_85_2","doi-asserted-by":"publisher","DOI":"10.1006\/jsbi.1999.4094"},{"key":"e_1_3_2_86_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444904019158"},{"key":"e_1_3_2_87_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0108767386099622"},{"key":"e_1_3_2_88_2","doi-asserted-by":"publisher","DOI":"10.1107\/S0021889891004399"},{"key":"e_1_3_2_89_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0076-6879(97)77028-9"},{"key":"e_1_3_2_90_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msn067"},{"key":"e_1_3_2_91_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msy096"},{"key":"e_1_3_2_92_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkr245"},{"key":"e_1_3_2_93_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkv1164"},{"key":"e_1_3_2_94_2","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a040023"}],"container-title":["mBio"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mBio.00009-19","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mBio.00009-19","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,15]],"date-time":"2024-07-15T06:05:09Z","timestamp":1721023509000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/mBio.00009-19"}},"subtitle":[],"editor":[{"given":"Nancy E.","family":"Freitag","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2019,4,30]]},"references-count":93,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2019,4,30]]}},"alternative-id":["10.1128\/mBio.00009-19"],"URL":"https:\/\/doi.org\/10.1128\/mbio.00009-19","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/369546","asserted-by":"object"}]},"ISSN":["2161-2129","2150-7511"],"issn-type":[{"value":"2161-2129","type":"print"},{"value":"2150-7511","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,4,30]]},"assertion":[{"value":"2019-01-02","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2019-01-29","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2019-03-05","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e00009-19"}}