{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T15:55:09Z","timestamp":1789055709521,"version":"build-2803163510"},"reference-count":58,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2026,5,8]],"date-time":"2026-05-08T00:00:00Z","timestamp":1778198400000},"content-version":"vor","delay-in-days":127,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100014013","name":"UKRI","doi-asserted-by":"publisher","award":["MR\/W031361\/1"],"award-info":[{"award-number":["MR\/W031361\/1"]}],"id":[{"id":"10.13039\/100014013","id-type":"DOI","asserted-by":"publisher"}]},{"name":"JPIAMR-Joint Programming Initiative on Antimicrobial Resistance"},{"name":"UKRI Frontiers","award":["EP\/Y031067\/1"],"award-info":[{"award-number":["EP\/Y031067\/1"]}]},{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/T008784\/1"],"award-info":[{"award-number":["BB\/T008784\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,1,14]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Phage therapy offers an alternative to antibiotics for treating multidrug-resistant infections. Plasmid-dependent phages (PDPs) are promising therapeutics as they can kill targeted pathogens and prevent the spread of plasmid-encoded antibiotic resistance genes. However, the evolutionary trajectories of multidrug-resistance (MDR) plasmids under the selective pressure of PDPs remain poorly understood, particularly in eco-evolutionary contexts that remain permissive to plasmid conjugation. We experimentally evolved populations of Escherichia coli carrying the MDR plasmid RP4 in the presence of the plasmid-dependent phage PRD1 under conditions where the benefits of conjugation were either strong or weak. When opportunities for conjugation were rare, PRD1 only transiently suppressed the conjugative plasmid population due to the rapid evolution of phage-resistant plasmids lacking conjugative ability. Increasing ecological opportunities for conjugation enhanced plasmid suppression and delayed the evolution of phage-resistant plasmids. PRD1 resistance was associated with plasmid loss and reduced conjugative ability, though this trade-off was complex because resistance mutations caused heterogeneous effects on pilus production and conjugation. Mutations and insertion sequence (IS)-mediated inactivation in conjugation genes generated a spectrum of resistance phenotypes, from partial (trbB, trbL) to complete (virB4\/trbE) resistance. Bioinformatic analysis of publicly available IncP plasmids revealed frequent truncations of the VirB4\/TrbE protein, suggesting that plasmid-dependent phages may represent an important selective pressure shaping plasmid evolution in natural populations. Our results demonstrate an evolutionary trade-off between conjugative ability and phage resistance that plasmids cannot easily circumvent. Targeting multidrug-resistance plasmids with PDPs is likely to drive loss of conjugation, limiting the transfer of antibiotic resistance genes in microbial communities.<\/jats:p>","DOI":"10.1093\/ismejo\/wrag113","type":"journal-article","created":{"date-parts":[[2026,5,6]],"date-time":"2026-05-06T11:39:39Z","timestamp":1778067579000},"source":"Crossref","is-referenced-by-count":2,"title":["Eco-evolutionary responses to plasmid-dependent phage constrain the spread of multidrug-resistance plasmids"],"prefix":"10.1093","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6667-3780","authenticated-orcid":false,"given":"Daniel","family":"Cazares","sequence":"first","affiliation":[{"name":"Department of Biology, University of Oxford , Life and Mind Building, South Parks Road, Oxford, Oxfordshire OX1 3EL ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eliza","family":"Rayner","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Oxford , Life and Mind Building, South Parks Road, Oxford, Oxfordshire OX1 3EL ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6242-4405","authenticated-orcid":false,"given":"Adrian","family":"Cazares","sequence":"additional","affiliation":[{"name":"Parasites and Microbes Programme, Wellcome Sanger Institute , Hinxton CB10 1SA ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0882-5106","authenticated-orcid":false,"given":"Wendy","family":"Figueroa","sequence":"additional","affiliation":[{"name":"Parasites and Microbes Programme, Wellcome Sanger Institute , Hinxton CB10 1SA ,","place":["United Kingdom"]},{"name":"Department of Medicine, University of Cambridge , Cambridge CB2 0BB ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Goulding","sequence":"additional","affiliation":[{"name":"Parasites and Microbes Programme, Wellcome Sanger Institute , Hinxton CB10 1SA ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4748-6792","authenticated-orcid":false,"given":"Samuel T E","family":"Greenrod","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Oxford , Life and Mind Building, South Parks Road, Oxford, Oxfordshire OX1 3EL ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5246-6617","authenticated-orcid":false,"given":"Adam J","family":"Mulkern","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Oxford , Life and Mind Building, South Parks Road, Oxford, Oxfordshire OX1 3EL ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4694-6673","authenticated-orcid":false,"given":"Michelle Y Y","family":"Yin","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Oxford , Life and Mind Building, South Parks Road, Oxford, Oxfordshire OX1 3EL ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tao","family":"He","sequence":"additional","affiliation":[{"name":"Jiangsu Academy of Agricultural Sciences , Nanjing 210040 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4432-8505","authenticated-orcid":false,"given":"Nick","family":"Thomson","sequence":"additional","affiliation":[{"name":"Parasites and Microbes Programme, Wellcome Sanger Institute , Hinxton CB10 1SA ,","place":["United Kingdom"]},{"name":"Department of Pathogen Molecular Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine , Keppel Street, London WC1E 7HT ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0362-820X","authenticated-orcid":false,"given":"Michael A","family":"Brockhurst","sequence":"additional","affiliation":[{"name":"Division of Evolution, Infection and Genomics, Faculty of Biology, Medicine and Health, University of Manchester , Manchester M13 9NT ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7941-813X","authenticated-orcid":false,"given":"R Craig","family":"MacLean","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Oxford , Life and Mind Building, South Parks Road, Oxford, Oxfordshire OX1 3EL ,","place":["United Kingdom"]},{"name":"All Souls College , High Street, Oxford OX1 4AL ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,5,8]]},"reference":[{"key":"2026053109514364100_ref1","doi-asserted-by":"publisher","first-page":"1082","DOI":"10.1126\/science.aax3879","article-title":"The evolution of antibiotic resistance","volume":"365","author":"MacLean","year":"2019","journal-title":"Science"},{"key":"2026053109514364100_ref2","doi-asserted-by":"publisher","first-page":"e00088","DOI":"10.1128\/CMR.00088-17","article-title":"Mobile genetic elements associated with antimicrobial resistance","volume":"31","author":"Partridge","year":"2018","journal-title":"Clin Microbiol Rev"},{"key":"2026053109514364100_ref3","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1111\/eva.12202","article-title":"The genetic basis of the fitness costs of antimicrobial resistance: a meta-analysis approach","volume":"8","author":"Vogwill","year":"2015","journal-title":"Evol Appl"},{"key":"2026053109514364100_ref4","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1093\/genetics\/113.3.483","article-title":"Transitory derepression and the maintenance of conjugative plasmids","volume":"113","author":"Lundquist","year":"1986","journal-title":"Genetics"},{"key":"2026053109514364100_ref5","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1093\/genetics\/94.2.425","article-title":"The population biology of bacterial plasmids: a priori conditions for the existence of mobilizable nonconjugative factors","volume":"94","author":"Levin","year":"1980","journal-title":"Genetics"},{"key":"2026053109514364100_ref6","doi-asserted-by":"publisher","first-page":"1689","DOI":"10.1038\/s41467-017-01532-1","article-title":"Persistence and reversal of plasmid-mediated antibiotic resistance","volume":"8","author":"Lopatkin","year":"2017","journal-title":"Nat Commun"},{"key":"2026053109514364100_ref7","doi-asserted-by":"publisher","first-page":"1348","DOI":"10.1038\/s41559-017-0250-3","article-title":"Positive selection inhibits gene mobilization and transfer in soil bacterial communities","volume":"1","author":"Hall","year":"2017","journal-title":"Nat Ecol Evol"},{"key":"2026053109514364100_ref8","doi-asserted-by":"publisher","first-page":"8260","DOI":"10.1073\/pnas.1600974113","article-title":"Source\u2013sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities","volume":"113","author":"Hall","year":"2016","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2026053109514364100_ref9","doi-asserted-by":"publisher","first-page":"2653","DOI":"10.1038\/s41467-021-22849-y","article-title":"Variability of plasmid fitness effects contributes to plasmid persistence in bacterial communities","volume":"12","author":"Alonso-del Valle","year":"2021","journal-title":"Nat Commun"},{"key":"2026053109514364100_ref10","doi-asserted-by":"publisher","first-page":"606","DOI":"10.1038\/s41564-021-00879-y","article-title":"Pervasive transmission of a carbapenem resistance plasmid in the gut microbiota of hospitalized patients","volume":"6","author":"Le\u00f3n-Sampedro","year":"2021","journal-title":"Nat Microbiol"},{"key":"2026053109514364100_ref11","doi-asserted-by":"publisher","first-page":"343ra81","DOI":"10.1126\/scitranslmed.aad0917","article-title":"Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability","volume":"8","author":"Yassour","year":"2016","journal-title":"Sci Transl Med"},{"key":"2026053109514364100_ref12","doi-asserted-by":"publisher","first-page":"2058","DOI":"10.1038\/s41396-023-01509-7","article-title":"Regulatory fine-tuning of mcr-1 increases bacterial fitness and stabilises antibiotic resistance in agricultural settings","volume":"17","author":"Ogunlana","year":"2023","journal-title":"ISME J"},{"key":"2026053109514364100_ref13","doi-asserted-by":"publisher","first-page":"6924","DOI":"10.1038\/s41467-024-51398-3","article-title":"Insights into the ecology of the infant gut plasmidome","volume":"15","author":"He","year":"2024","journal-title":"Nat Commun"},{"key":"2026053109514364100_ref14","doi-asserted-by":"publisher","first-page":"1516","DOI":"10.1038\/s41564-022-01221-w","article-title":"Long-term ecological and evolutionary dynamics in the gut microbiomes of carbapenemase-producing Enterobacteriaceae colonized subjects","volume":"7","author":"Kang","year":"2022","journal-title":"Nat Microbiol"},{"key":"2026053109514364100_ref15","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1038\/s41587-019-0105-3","article-title":"Engineered toxin\u2013intein antimicrobials can selectively target and kill antibiotic-resistant bacteria in mixed populations","volume":"37","author":"L\u00f3pez-Igual","year":"2019","journal-title":"Nat Biotechnol"},{"key":"2026053109514364100_ref16","doi-asserted-by":"publisher","first-page":"gkaf275","DOI":"10.1093\/nar\/gkaf275","article-title":"Activation, incompatibility, and displacement of FIB replicons in E. coli","volume":"53","author":"Lloyd","year":"2025","journal-title":"Nucleic Acids Res"},{"key":"2026053109514364100_ref17","doi-asserted-by":"publisher","first-page":"12282","DOI":"10.1073\/pnas.0702760104","article-title":"Disrupting antibiotic resistance propagation by inhibiting the conjugative DNA relaxase","volume":"104","author":"Lujan","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2026053109514364100_ref18","doi-asserted-by":"publisher","first-page":"e01032","DOI":"10.1128\/mBio.01032-15","article-title":"Synthetic fatty acids prevent plasmid-mediated horizontal gene transfer","volume":"6","author":"Getino","year":"2015","journal-title":"mBio"},{"key":"2026053109514364100_ref19","doi-asserted-by":"publisher","first-page":"eabe3868","DOI":"10.1126\/sciadv.abe3868","article-title":"Niche and local geography shape the pangenome of wastewater- and livestock-associated Enterobacteriaceae","volume":"7","author":"Shaw","year":"2021","journal-title":"Sci Adv"},{"key":"2026053109514364100_ref20","doi-asserted-by":"publisher","first-page":"1161","DOI":"10.1016\/S1473-3099(20)30149-3","article-title":"Changes in colistin resistance and mcr-1 abundance in Escherichia coli of animal and human origins following the ban of colistin-positive additives in China: an epidemiological comparative study","volume":"20","author":"Wang","year":"2020","journal-title":"Lancet Infect Dis"},{"key":"2026053109514364100_ref21","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1016\/S1473-3099(10)70143-2","article-title":"Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study","volume":"10","author":"Kumarasamy","year":"2010","journal-title":"Lancet Infect Dis"},{"key":"2026053109514364100_ref22","doi-asserted-by":"publisher","first-page":"280","DOI":"10.3390\/microorganisms9020280","article-title":"Indirect selection against antibiotic resistance via specialized plasmid-dependent bacteriophages","volume":"9","author":"Penttinen","year":"2021","journal-title":"Microorganisms"},{"key":"2026053109514364100_ref23","doi-asserted-by":"publisher","first-page":"2535","DOI":"10.1099\/00221287-134-9-2535","article-title":"Bacteriophage X-2: a filamentous phage lysing IncX-plasmid-harbouring bacterial strains","volume":"134","author":"Coetzee","year":"1988","journal-title":"Microbiology"},{"key":"2026053109514364100_ref24","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1099\/00221287-126-2-389","article-title":"Phage X: a plasmid-dependent, broad host range, filamentous bacterial virus","volume":"126","author":"Bradley","year":"1981","journal-title":"Microbiology"},{"key":"2026053109514364100_ref25","doi-asserted-by":"publisher","first-page":"689","DOI":"10.1128\/jvi.14.3.689-699.1974","article-title":"Characteristics of PRD1, a plasmid-dependent broad host range DNA bacteriophage","volume":"14","author":"Olsen","year":"1974","journal-title":"J Virol"},{"key":"2026053109514364100_ref26","doi-asserted-by":"publisher","first-page":"e0253723","DOI":"10.1128\/spectrum.02537-23","article-title":"Isolation and characterization of novel plasmid-dependent phages infecting bacteria carrying diverse conjugative plasmids","volume":"12","author":"Parra","year":"2024","journal-title":"Microbiol Spectrum"},{"key":"2026053109514364100_ref27","doi-asserted-by":"publisher","first-page":"4733","DOI":"10.1128\/jb.179.15.4733-4740.1997","article-title":"Assembly of a functional phage PRD1 receptor depends on 11 genes of the IncP plasmid mating pair formation complex","volume":"179","author":"Grahn","year":"1997","journal-title":"J Bacteriol"},{"key":"2026053109514364100_ref28","doi-asserted-by":"publisher","first-page":"3197","DOI":"10.1038\/s41467-024-47416-z","article-title":"Diverse and abundant phages exploit conjugative plasmids","volume":"15","author":"Quinones-Olvera","year":"2024","journal-title":"Nat Commun"},{"key":"2026053109514364100_ref29","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.1038\/s41467-022-28819-2","article-title":"Role of mobile genetic elements in the global dissemination of the carbapenem resistance gene blaNDM","volume":"13","author":"Acman","year":"2022","journal-title":"Nat Commun"},{"key":"2026053109514364100_ref30","doi-asserted-by":"publisher","first-page":"1179","DOI":"10.1038\/s41467-018-03205-z","article-title":"The global distribution and spread of the mobilized colistin resistance gene mcr-1","volume":"9","author":"Wang","year":"2018","journal-title":"Nat Commun"},{"key":"2026053109514364100_ref31","doi-asserted-by":"publisher","first-page":"12616","DOI":"10.1038\/s41598-019-48483-9","article-title":"Sex pilus specific bacteriophage to drive bacterial population towards antibiotic sensitivity","volume":"9","author":"Colom","year":"2019","journal-title":"Sci Rep"},{"key":"2026053109514364100_ref32","doi-asserted-by":"publisher","first-page":"902","DOI":"10.1098\/rsbl.2011.0384","article-title":"Bacteriophage selection against a plasmid-encoded sex apparatus leads to the loss of antibiotic-resistance plasmids","volume":"7","author":"Jalasvuori","year":"2011","journal-title":"Biol Lett"},{"key":"2026053109514364100_ref33","doi-asserted-by":"publisher","first-page":"1434","DOI":"10.1038\/s41564-024-01705-x","article-title":"Personalized bacteriophage therapy outcomes for 100 consecutive cases: a multicentre, multinational, retrospective observational study","volume":"9","author":"Pirnay","year":"2024","journal-title":"Nat Microbiol"},{"key":"2026053109514364100_ref34","doi-asserted-by":"publisher","first-page":"msac115","DOI":"10.1093\/molbev\/msac115","article-title":"Evolution of plasmid mobility: origin and fate of conjugative and nonconjugative plasmids","volume":"39","author":"Coluzzi","year":"2022","journal-title":"Mol Biol Evol"},{"key":"2026053109514364100_ref35","doi-asserted-by":"publisher","first-page":"e2107818118","DOI":"10.1073\/pnas.2107818118","article-title":"Increased copy number couples the evolution of plasmid horizontal transmission and plasmid-encoded antibiotic resistance","volume":"118","author":"Dimitriu","year":"2021","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2026053109514364100_ref36","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1017\/S0031182000055360","article-title":"Coevolution of hosts and parasites","volume":"85","author":"Anderson","year":"1982","journal-title":"Parasitology"},{"key":"2026053109514364100_ref37","doi-asserted-by":"publisher","first-page":"2860","DOI":"10.1093\/molbev\/msw163","article-title":"Survival and evolution of a large multidrug resistance plasmid in new clinical bacterial hosts","volume":"33","author":"Porse","year":"2016","journal-title":"Mol Biol Evol"},{"key":"2026053109514364100_ref38","doi-asserted-by":"publisher","first-page":"e0253722","DOI":"10.1128\/mbio.02537-22","article-title":"Off-target integron activity leads to rapid plasmid compensatory evolution in response to antibiotic selection pressure","volume":"14","author":"Souque","year":"2023","journal-title":"mBio"},{"key":"2026053109514364100_ref39","doi-asserted-by":"publisher","DOI":"10.1128\/microbiolspec.MTBP-0016-2017","article-title":"Fitness costs of plasmids: a limit to plasmid transmission","volume":"5","author":"San","year":"2017","journal-title":"Microbiol Spectrum"},{"key":"2026053109514364100_ref40","doi-asserted-by":"publisher","first-page":"e102","DOI":"10.1002\/cpbi.102","article-title":"Using SPAdes De Novo Assembler","volume":"70","author":"Prjibelski","year":"2020","journal-title":"CP Bioinformatics"},{"key":"2026053109514364100_ref41","doi-asserted-by":"publisher","first-page":"1243","DOI":"10.1038\/nature08480","article-title":"Genome evolution and adaptation in a long-term experiment with Escherichia coli","volume":"461","author":"Barrick","year":"2009","journal-title":"Nature"},{"key":"2026053109514364100_ref42","doi-asserted-by":"publisher","first-page":"000685","DOI":"10.1099\/mgen.0.000685","article-title":"Bakta: rapid and standardized annotation of bacterial genomes via alignment-free sequence identification: find out more about Bakta, the motivation, challenges and applications, here","volume":"7","author":"Schwengers","year":"2021","journal-title":"Microb Genom"},{"key":"2026053109514364100_ref43","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1038\/s41592-022-01488-1","article-title":"ColabFold: making protein folding accessible to all","volume":"19","author":"Mirdita","year":"2022","journal-title":"Nat Methods"},{"key":"2026053109514364100_ref44","doi-asserted-by":"publisher","first-page":"e4792","DOI":"10.1002\/pro.4792","article-title":"UCSF ChimeraX: tools for structure building and analysis","volume":"32","author":"Meng","year":"2023","journal-title":"Protein Sci"},{"key":"2026053109514364100_ref45","doi-asserted-by":"publisher","first-page":"eadr1522","DOI":"10.1126\/science.adr1522","article-title":"Pre- and postantibiotic epoch: the historical spread of antimicrobial resistance","volume":"390","author":"Cazares","year":"2025","journal-title":"Science"},{"key":"2026053109514364100_ref46","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J Mol Biol"},{"key":"2026053109514364100_ref47","doi-asserted-by":"publisher","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"Edgar","year":"2004","journal-title":"Nucleic Acids Res"},{"key":"2026053109514364100_ref48","doi-asserted-by":"publisher","first-page":"1972","DOI":"10.1093\/bioinformatics\/btp348","article-title":"trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses","volume":"25","author":"Capella-Guti\u00e9rrez","year":"2009","journal-title":"Bioinformatics"},{"key":"2026053109514364100_ref49","doi-asserted-by":"publisher","first-page":"4453","DOI":"10.1093\/bioinformatics\/btz305","article-title":"RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference","volume":"35","author":"Kozlov","year":"2019","journal-title":"Bioinformatics"},{"key":"2026053109514364100_ref50","doi-asserted-by":"publisher","first-page":"W78","DOI":"10.1093\/nar\/gkae268","article-title":"Interactive tree of life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool","volume":"52","author":"Letunic","year":"2024","journal-title":"Nucleic Acids Res"},{"key":"2026053109514364100_ref51","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1111\/j.1574-6976.1998.tb00355.x","article-title":"Control of genes for conjugative transfer of plasmids and other mobile elements","volume":"21","author":"Zatyka","year":"1998","journal-title":"FEMS Microbiol Rev"},{"key":"2026053109514364100_ref52","doi-asserted-by":"publisher","first-page":"2097","DOI":"10.1038\/s41559-024-02523-4","article-title":"Plasmid-encoded insertion sequences promote rapid adaptation in clinical enterobacteria","volume":"8","author":"Sastre-Dominguez","year":"2024","journal-title":"Nat Ecol Evol"},{"key":"2026053109514364100_ref53","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1038\/s41586-022-04859-y","article-title":"Cryo-EM structure of a type IV secretion system","volume":"607","author":"Mac\u00e9","year":"2022","journal-title":"Nature"},{"key":"2026053109514364100_ref54","doi-asserted-by":"publisher","first-page":"3089","DOI":"10.1128\/jb.175.10.3089-3095.1993","article-title":"Binding of an Escherichia coli double-stranded DNA virus PRD1 to a receptor coded by an IncP-type plasmid","volume":"175","author":"Kotilainen","year":"1993","journal-title":"J Bacteriol"},{"key":"2026053109514364100_ref55","doi-asserted-by":"publisher","first-page":"1505","DOI":"10.1093\/genetics\/155.4.1505","article-title":"Natural selection, infectious transfer and the existence conditions for bacterial plasmids","volume":"155","author":"Bergstrom","year":"2000","journal-title":"Genetics"},{"key":"2026053109514364100_ref56","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1126\/science.aam9974","article-title":"High parasite diversity accelerates host adaptation and diversification","volume":"360","author":"Betts","year":"2018","journal-title":"Science"},{"key":"2026053109514364100_ref57","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1038\/nature08798","article-title":"Antagonistic coevolution accelerates molecular evolution","volume":"464","author":"Paterson","year":"2010","journal-title":"Nature"},{"key":"2026053109514364100_ref58","doi-asserted-by":"publisher","first-page":"670","DOI":"10.1038\/s41579-024-01102-5","article-title":"Rediscovering plasmid-dependent phages","volume":"22","author":"Cazares","year":"2024","journal-title":"Nat Rev Microbiol"}],"container-title":["The ISME Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/ismej\/advance-article-pdf\/doi\/10.1093\/ismejo\/wrag113\/68251821\/wrag113.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ismej\/article-pdf\/20\/1\/wrag113\/68251821\/wrag113.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ismej\/article-pdf\/20\/1\/wrag113\/68251821\/wrag113.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,31]],"date-time":"2026-05-31T13:51:49Z","timestamp":1780235509000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ismej\/article\/doi\/10.1093\/ismejo\/wrag113\/8673213"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1]]},"references-count":58,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2026,1,14]]}},"URL":"https:\/\/doi.org\/10.1093\/ismejo\/wrag113","relation":{},"ISSN":["1751-7362","1751-7370"],"issn-type":[{"value":"1751-7362","type":"print"},{"value":"1751-7370","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2026,1]]},"published":{"date-parts":[[2026,1]]},"article-number":"wrag113"}}