{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T20:36:20Z","timestamp":1792528580761,"version":"4.5.0"},"reference-count":75,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2025,4,6]],"date-time":"2025-04-06T00:00:00Z","timestamp":1743897600000},"content-version":"vor","delay-in-days":95,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["ArtRNA, CoG-101088027"],"award-info":[{"award-number":["ArtRNA, CoG-101088027"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Mukoviszidose Institut GmbH","award":["P2201"],"award-info":[{"award-number":["P2201"]}]},{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","award":["ANR-19-AMRB-0002"],"award-info":[{"award-number":["ANR-19-AMRB-0002"]}],"id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","award":["\u2018MAPVAP\u2019, FKZ 01KI2124"],"award-info":[{"award-number":["\u2018MAPVAP\u2019, FKZ 01KI2124"]}],"id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche, France","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,1,2]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Virulent bacteriophages (or phages) are viruses that specifically infect and lyse a bacterial host. When multiple phages co-infect a bacterial host, the extent of lysis and dynamics of bacteria\u2013phage and phage\u2013phage interactions are expected to vary. The objective of this study is to identify the factors influencing the interaction of two virulent phages with different Pseudomonas aeruginosa growth states (planktonic, an infected epithelial cell line, and biofilm) by measuring the bacterial time-kill and individual phage replication kinetics. A single administration of phages effectively reduced P. aeruginosa viability in planktonic conditions and infected human lung cell cultures, but phage-resistant variants subsequently emerged. In static biofilms, the phage combination displayed initial inhibition of biofilm dispersal, but sustained control was achieved only by combining phages and the meropenem antibiotic. In contrast, adherent biofilms showed tolerance to phage and\/or meropenem, suggesting a spatio-temporal variation in the phage\u2013bacterial interaction. The kinetics of adsorption of each phage to P. aeruginosa during single or co-administration were comparable. However, the phage with the shorter lysis time depleted bacterial resources early and selected a specific nucleotide polymorphism that conferred a competitive disadvantage and cross-resistance to the second phage. The extent and strength of this phage\u2013phage competition and genetic loci conferring phage resistance are, however, P. aeruginosa genotype-dependent. Nevertheless, adding phages sequentially resulted in their unimpeded replication with no significant increase in bacterial host lysis. These results highlight the interrelatedness of phage\u2013phage competition, phage resistance, and specific bacterial growth state (planktonic\/biofilm) in shaping the interplay among P. aeruginosa and virulent phages.<\/jats:p>","DOI":"10.1093\/ismejo\/wraf065","type":"journal-article","created":{"date-parts":[[2025,4,6]],"date-time":"2025-04-06T15:58:06Z","timestamp":1743955086000},"source":"Crossref","is-referenced-by-count":25,"title":["Phage\u2013phage competition and biofilms affect interactions between two virulent bacteriophages and\n                    <i>Pseudomonas aeruginosa<\/i>"],"prefix":"10.1093","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4767-2942","authenticated-orcid":false,"given":"Magdalena","family":"B\u00fcrkle","sequence":"first","affiliation":[{"name":"Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , 10117 Berlin ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6073-9307","authenticated-orcid":false,"given":"Imke H E","family":"Korf","sequence":"additional","affiliation":[{"name":"Pharmaceutical Biotechnology, Fraunhofer Institute for Toxicology and Experimental Medicine , 38124 Braunschweig ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8492-1947","authenticated-orcid":false,"given":"Anne","family":"Lippegaus","sequence":"additional","affiliation":[{"name":"General Microbiology, Institute of Microbiology, Friedrich Schiller University , 07745 Jena ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9413-5701","authenticated-orcid":false,"given":"Sebastian","family":"Krautwurst","sequence":"additional","affiliation":[{"name":"General Microbiology, Institute of Microbiology, Friedrich Schiller University , 07745 Jena ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Rohde","sequence":"additional","affiliation":[{"name":"Clinical Phages and Regulations, Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures , 38124 Braunschweig ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3701-3190","authenticated-orcid":false,"given":"Chantal","family":"Weissfuss","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , 10117 Berlin ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1973-3119","authenticated-orcid":false,"given":"Geraldine","family":"Nouailles","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , 10117 Berlin ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xavi\u00e8re Menatong","family":"Tene","sequence":"additional","affiliation":[{"name":"Bacteriophage Bacterium Host, Department of Microbiology, Institut Pasteur, Universit\u00e9 Paris-Cit\u00e9, CNRS UMR6047 , 75015 Paris ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9586-3014","authenticated-orcid":false,"given":"Baptiste","family":"Gaborieau","sequence":"additional","affiliation":[{"name":"Bacteriophage Bacterium Host, Department of Microbiology, Institut Pasteur, Universit\u00e9 Paris-Cit\u00e9, CNRS UMR6047 , 75015 Paris ,","place":["France"]},{"name":"Infection Antimicrobials Modelling Evolution, Universit\u00e9 Paris Cit\u00e9, Inserm, UMR 1137 , 75018 Paris ,","place":["France"]},{"name":"DMU ESPRIT, M\u00e9decine Intensive R\u00e9animation, APHP, H\u00f4pital Louis Mourier , 92700 Colombes ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6528-118X","authenticated-orcid":false,"given":"Jean-Marc","family":"Ghigo","sequence":"additional","affiliation":[{"name":"Genetics of Biofilms Laboratory, Department of Microbiology, Institut Pasteur, Universit\u00e9 Paris-Cit\u00e9, UMR CNRS 6047 , 75015 Paris ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1828-2299","authenticated-orcid":false,"given":"Jean-Damien","family":"Ricard","sequence":"additional","affiliation":[{"name":"Infection Antimicrobials Modelling Evolution, Universit\u00e9 Paris Cit\u00e9, Inserm, UMR 1137 , 75018 Paris ,","place":["France"]},{"name":"DMU ESPRIT, M\u00e9decine Intensive R\u00e9animation, APHP, H\u00f4pital Louis Mourier , 92700 Colombes ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6935-8612","authenticated-orcid":false,"given":"Andreas C","family":"Hocke","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , 10117 Berlin ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5560-9804","authenticated-orcid":false,"given":"Kai","family":"Papenfort","sequence":"additional","affiliation":[{"name":"General Microbiology, Institute of Microbiology, Friedrich Schiller University , 07745 Jena ,","place":["Germany"]},{"name":"Microverse Cluster, Friedrich Schiller University Jena , 07745 Jena ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6875-5758","authenticated-orcid":false,"given":"Laurent","family":"Debarbieux","sequence":"additional","affiliation":[{"name":"Bacteriophage Bacterium Host, Department of Microbiology, Institut Pasteur, Universit\u00e9 Paris-Cit\u00e9, CNRS UMR6047 , 75015 Paris ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9787-5633","authenticated-orcid":false,"given":"Martin","family":"Witzenrath","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , 10117 Berlin ,","place":["Germany"]},{"name":"German Center for Lung Research (DZL) , Berlin ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5655-4350","authenticated-orcid":false,"given":"Sandra-Maria","family":"Wienhold","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , 10117 Berlin ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0617-6897","authenticated-orcid":false,"given":"Gopinath","family":"Krishnamoorthy","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, Respiratory Medicine and Critical Care, Charit\u00e9 \u2013 Universit\u00e4tsmedizin Berlin, Corporate Member of Freie Universit\u00e4t Berlin and Humboldt-Universit\u00e4t zu Berlin , 10117 Berlin ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,4,6]]},"reference":[{"key":"2025043001414106400_ref1","doi-asserted-by":"publisher","first-page":"e00138","DOI":"10.1128\/cmr.00138-18","article-title":"Cystic fibrosis and Pseudomonas aeruginosa: the host-microbe interface","volume":"32","author":"Malhotra","year":"2019","journal-title":"Clin Microbiol Rev"},{"key":"2025043001414106400_ref2","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1038\/s41579-022-00767-0","article-title":"The biofilm life cycle: expanding the conceptual model of biofilm formation","volume":"20","author":"Sauer","year":"2022","journal-title":"Nat Rev Microbiol"},{"key":"2025043001414106400_ref3","doi-asserted-by":"publisher","first-page":"510","DOI":"10.1128\/MMBR.00013-14","article-title":"Biofilm-related infections: bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics","volume":"78","author":"Lebeaux","year":"2014","journal-title":"Microbiol Mol Biol Rev"},{"key":"2025043001414106400_ref4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1472-6785-6-19","article-title":"The impact of phages on interspecific competition in experimental populations of bacteria","volume":"6","author":"Brockhurst","year":"2006","journal-title":"BMC Ecol"},{"key":"2025043001414106400_ref5","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1038\/s41579-021-00602-y","article-title":"Interactions between bacterial and phage communities in natural environments","volume":"20","author":"Chevallereau","year":"2022","journal-title":"Nat Rev Microbiol"},{"key":"2025043001414106400_ref6","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1146\/annurev-virology-091919-074222","article-title":"Understanding the complex phage-host interactions in biofilm communities","volume":"8","author":"Pires","year":"2021","journal-title":"Annu Rev Virol"},{"key":"2025043001414106400_ref7","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.mib.2019.03.005","article-title":"Stronger together? Perspectives on phage-antibiotic synergy in clinical applications of phage therapy","volume":"51","author":"Segall","year":"2019","journal-title":"Curr Opin Microbiol"},{"key":"2025043001414106400_ref8","doi-asserted-by":"publisher","first-page":"e03219","DOI":"10.1128\/spectrum.03219-23","article-title":"Exploiting phage-antibiotic synergies to disrupt Pseudomonas aeruginosa PAO1 biofilms in the context of orthopedic infections","volume":"12","author":"De Soir","year":"2024","journal-title":"Microbiol Spectr"},{"key":"2025043001414106400_ref9","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.chom.2017.06.018","article-title":"Synergy between the host immune system and bacteriophage is essential for successful phage therapy against an acute respiratory pathogen","volume":"22","author":"Roach","year":"2017","journal-title":"Cell Host Microbe"},{"key":"2025043001414106400_ref10","doi-asserted-by":"publisher","first-page":"e00062","DOI":"10.1128\/cmr.00062-22","article-title":"Reassessment of historical clinical trials supports the effectiveness of phage therapy","volume":"6","author":"Marongiu","year":"2022","journal-title":"Clin Microbiol Rev"},{"key":"2025043001414106400_ref11","doi-asserted-by":"publisher","first-page":"e00877","DOI":"10.1128\/mSystems.00877-19","article-title":"Biofilm structure promotes coexistence of phage-resistant and phage-susceptible bacteria","volume":"5","author":"Simmons","year":"2020","journal-title":"mSystems"},{"key":"2025043001414106400_ref12","doi-asserted-by":"publisher","first-page":"e65355","DOI":"10.7554\/eLife.65355","article-title":"Matrix-trapped viruses can prevent invasion of bacterial biofilms by colonizing cells","volume":"10","author":"Bond","year":"2021","journal-title":"elife"},{"key":"2025043001414106400_ref13","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1038\/ismej.2017.190","article-title":"Phage mobility is a core determinant of phage\u2013bacteria coexistence in biofilms","volume":"12","author":"Simmons","year":"2018","journal-title":"ISME J"},{"key":"2025043001414106400_ref14","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1038\/s41564-017-0050-1","article-title":"Dynamic biofilm architecture confers individual and collective mechanisms of viral protection","volume":"3","author":"Vidakovic","year":"2018","journal-title":"Nat Microbiol"},{"key":"2025043001414106400_ref15","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1007\/BF01570111","article-title":"Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes","volume":"16","author":"Doolittle","year":"1996","journal-title":"J Ind Microbiol"},{"key":"2025043001414106400_ref16","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1038\/s42003-019-0633-x","article-title":"Spatial structure affects phage efficacy in infecting dual-strain biofilms of Pseudomonas aeruginosa","volume":"2","author":"Testa","year":"2019","journal-title":"Commun Biol"},{"key":"2025043001414106400_ref17","doi-asserted-by":"publisher","first-page":"1057","DOI":"10.3390\/v14051057","article-title":"Deconstructing the phage\u2013bacterial biofilm interaction as a basis to establish new antibiofilm strategies","volume":"14","author":"Visnapuu","year":"2022","journal-title":"Viruses"},{"key":"2025043001414106400_ref18","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1038\/s41467-023-44157-3","article-title":"Phage Paride can kill dormant, antibiotic-tolerant cells of Pseudomonas aeruginosa by direct lytic replication","volume":"15","author":"Maffei","year":"2024","journal-title":"Nat Commun"},{"key":"2025043001414106400_ref19","doi-asserted-by":"publisher","first-page":"101193","DOI":"10.1016\/j.jbc.2021.101193","article-title":"RetS inhibits Pseudomonas aeruginosa biofilm formation by disrupting the canonical histidine kinase dimerization interface of GacS","volume":"297","author":"Kaler","year":"2021","journal-title":"J Biol Chem"},{"key":"2025043001414106400_ref20","doi-asserted-by":"publisher","first-page":"e00197","DOI":"10.1128\/jvi.00197-22","article-title":"RetS regulates phage infection in Pseudomonas aeruginosa via modulating the GacS\/GacA two-component system","volume":"96","author":"Xuan","year":"2022","journal-title":"J Virol"},{"key":"2025043001414106400_ref21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0378-1097(04)00041-2","article-title":"The interaction of phage and biofilms","volume":"232","author":"Sutherland","year":"2004","journal-title":"FEMS Microbiol Lett"},{"key":"2025043001414106400_ref22","doi-asserted-by":"publisher","first-page":"2458","DOI":"10.1038\/s41598-022-06422-1","article-title":"Systematic analysis of putative phage-phage interactions on minimum-sized phage cocktails","volume":"12","author":"Molina","year":"2022","journal-title":"Sci Rep"},{"key":"2025043001414106400_ref23","doi-asserted-by":"publisher","first-page":"1451","DOI":"10.1038\/ismej.2011.30","article-title":"Within-host competition determines reproductive success of temperate bacteriophages","volume":"5","author":"Refardt","year":"2011","journal-title":"ISME J"},{"key":"2025043001414106400_ref24","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/S0065-2504(04)37010-8","article-title":"Parasitism between co-infecting bacteriophages","volume":"37","author":"Turner","year":"2005","journal-title":"Adv Ecol Res"},{"key":"2025043001414106400_ref25","doi-asserted-by":"publisher","first-page":"R1011","DOI":"10.1016\/j.cub.2023.08.077","article-title":"Bacteriophage ecology: getting a head start on genomic competitors","volume":"33","author":"Igler","year":"2023","journal-title":"Curr Biol"},{"key":"2025043001414106400_ref26","doi-asserted-by":"publisher","first-page":"e00286","DOI":"10.1128\/aem.00286-24","article-title":"Warming alters life-history traits and competition in a phage community","volume":"90","author":"Greenrod","year":"2024","journal-title":"Appl Environ Microbiol"},{"key":"2025043001414106400_ref27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2180-11-102","article-title":"Sequencing and characterization of Pseudomonas aeruginosa phage JG004","volume":"11","author":"Garbe","year":"2011","journal-title":"BMC Microbiol"},{"key":"2025043001414106400_ref28","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2180-10-301","article-title":"Characterization of JG024, a Pseudomonas aeruginosa PB1-like broad host range phage under simulated infection conditions","volume":"10","author":"Garbe","year":"2010","journal-title":"BMC Microbiol"},{"key":"2025043001414106400_ref29","doi-asserted-by":"publisher","first-page":"1952","DOI":"10.1111\/j.1462-2920.2012.02719.x","article-title":"Pseudomonas aeruginosa population structure revisited under environmental focus: impact of water quality and phage pressure","volume":"14","author":"Selezska","year":"2012","journal-title":"Environ Microbiol"},{"key":"2025043001414106400_ref30","doi-asserted-by":"publisher","first-page":"e0117163","DOI":"10.1371\/journal.pone.0117163","article-title":"The search for therapeutic bacteriophages uncovers one new subfamily and two new genera of pseudomonas-infecting Myoviridae","volume":"10","author":"Henry","year":"2015","journal-title":"PLoS One"},{"key":"2025043001414106400_ref31","doi-asserted-by":"publisher","first-page":"e1220348","DOI":"10.1080\/21597081.2016.1220348","article-title":"Phage therapy dosing: the problem (s) with multiplicity of infection (MOI)","volume":"6","author":"Abedon","year":"2016","journal-title":"Bacteriophage"},{"key":"2025043001414106400_ref32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.virol.2021.05.011","article-title":"Plaque size tool: an automated plaque analysis tool for simplifying and standardising bacteriophage plaque morphology measurements","volume":"561","author":"Trofimova","year":"2021","journal-title":"Virology"},{"key":"2025043001414106400_ref33","doi-asserted-by":"publisher","first-page":"3417","DOI":"10.1128\/AEM.70.6.3417-3424.2004","article-title":"Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157: H7","volume":"70","author":"O'flynn","year":"2004","journal-title":"Appl Environ Microbiol"},{"key":"2025043001414106400_ref34","doi-asserted-by":"publisher","first-page":"e1006134","DOI":"10.1371\/journal.pgen.1006134","article-title":"Next-generation \u201c-omics\u201d approaches reveal a massive alteration of host RNA metabolism during bacteriophage infection of Pseudomonas aeruginosa","volume":"12","author":"Chevallereau","year":"2016","journal-title":"PLoS Genet"},{"key":"2025043001414106400_ref35","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1007\/978-1-60327-164-6_18","article-title":"Practical methods for determining phage growth parameters","volume":"501","author":"Hyman","year":"2009","journal-title":"Methods Mol Biol"},{"key":"2025043001414106400_ref36","doi-asserted-by":"publisher","first-page":"e1008214","DOI":"10.1371\/journal.pcbi.1008214","article-title":"Galaxy and Apollo as a biologist-friendly interface for high-quality cooperative phage genome annotation","volume":"16","author":"Ramsey","year":"2020","journal-title":"PLoS Comput Biol"},{"key":"2025043001414106400_ref37","doi-asserted-by":"publisher","first-page":"1166","DOI":"10.1093\/bioinformatics\/bts091","article-title":"Unipro UGENE: a unified bioinformatics toolkit","volume":"28","author":"Okonechnikov","year":"2012","journal-title":"Bioinformatics"},{"key":"2025043001414106400_ref38","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1093\/nar\/gkh152","article-title":"ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences","volume":"32","author":"Laslett","year":"2004","journal-title":"Nucleic Acids Res"},{"key":"2025043001414106400_ref39","doi-asserted-by":"publisher","first-page":"955","DOI":"10.1093\/nar\/25.5.955","article-title":"tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence","volume":"25","author":"Lowe","year":"1997","journal-title":"Nucleic Acids Res"},{"key":"2025043001414106400_ref40","doi-asserted-by":"publisher","first-page":"10501","DOI":"10.1128\/JVI.01347-14","article-title":"Development of giant bacteriophage \u03d5KZ is independent of the host transcription apparatus","volume":"88","author":"Ceyssens","year":"2014","journal-title":"J Virol"},{"key":"2025043001414106400_ref41","doi-asserted-by":"publisher","first-page":"101290","DOI":"10.1016\/j.coviro.2022.101290","article-title":"The role of the animal host in the management of bacteriophage resistance during phage therapy","volume":"58","author":"Gaborieau","year":"2023","journal-title":"Curr Opin Virol"},{"key":"2025043001414106400_ref42","doi-asserted-by":"publisher","first-page":"2916","DOI":"10.1128\/iai.68.5.2916-2924.2000","article-title":"Pseudomonas aeruginosa cystic fibrosis isolates induce rapid, type III secretion-dependent, but ExoU-independent, oncosis of macrophages and polymorphonuclear neutrophils","volume":"68","author":"Dacheux","year":"2000","journal-title":"Infect Immun"},{"key":"2025043001414106400_ref43","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1111\/j.1752-4571.2008.00055.x","article-title":"Coinfection rates in \u03c66 bacteriophage are enhanced by virus-induced changes in host cells","volume":"2","author":"Joseph","year":"2009","journal-title":"Evol Appl"},{"key":"2025043001414106400_ref44","doi-asserted-by":"publisher","first-page":"e1010125","DOI":"10.1371\/journal.pcbi.1010125","article-title":"Superinfection exclusion: a viral strategy with short-term benefits and long-term drawbacks","volume":"18","author":"Hunter","year":"2022","journal-title":"PLoS Comput Biol"},{"key":"2025043001414106400_ref45","doi-asserted-by":"publisher","first-page":"e3897","DOI":"10.1371\/journal.pone.0003897","article-title":"Identification of biofilm-associated cluster (bac) in Pseudomonas aeruginosa involved in biofilm formation and virulence","volume":"3","author":"Mac\u00e9","year":"2008","journal-title":"PLoS One"},{"key":"2025043001414106400_ref46","doi-asserted-by":"publisher","first-page":"1306","DOI":"10.1128\/JB.01463-13","article-title":"Influence of O polysaccharides on biofilm development and outer membrane vesicle biogenesis in Pseudomonas aeruginosa PAO1","volume":"196","author":"Murphy","year":"2014","journal-title":"J Bacteriol"},{"key":"2025043001414106400_ref47","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1038\/s42005-023-01272-3","article-title":"The bacterial lectin LecA from P. Aeruginosa alters membrane organization by dispersing ordered domains","volume":"6","author":"Sych","year":"2023","journal-title":"Commun Phys"},{"key":"2025043001414106400_ref48","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2164-11-587","article-title":"Gene expression in Pseudomonas aeruginosa swarming motility","volume":"11","author":"Tremblay","year":"2010","journal-title":"BMC Genomics"},{"key":"2025043001414106400_ref49","doi-asserted-by":"publisher","first-page":"1778","DOI":"10.1080\/15476286.2020.1870844","article-title":"Differential transcription profiling of the phage LUZ19 infection process in different growth media","volume":"18","author":"Brand\u00e3o","year":"2021","journal-title":"RNA Biol"},{"key":"2025043001414106400_ref50","doi-asserted-by":"publisher","first-page":"1099","DOI":"10.1080\/15476286.2020.1827785","article-title":"Introducing differential RNA-seq mapping to track the early infection phase for pseudomonas phage \u0278KZ","volume":"18","author":"Wicke","year":"2021","journal-title":"RNA Biol"},{"key":"2025043001414106400_ref51","doi-asserted-by":"publisher","first-page":"2165","DOI":"10.1111\/1462-2920.14979","article-title":"Integrative omics analysis of Pseudomonas aeruginosa virus PA5oct highlights the molecular complexity of jumbo phages","volume":"22","author":"Lood","year":"2020","journal-title":"Environ Microbiol"},{"key":"2025043001414106400_ref52","doi-asserted-by":"publisher","first-page":"3128","DOI":"10.1111\/j.1462-2920.2011.02595.x","article-title":"The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling","volume":"13","author":"Moscoso","year":"2011","journal-title":"Environ Microbiol"},{"key":"2025043001414106400_ref53","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1016\/j.devcel.2004.08.020","article-title":"A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa","volume":"7","author":"Goodman","year":"2004","journal-title":"Dev Cell"},{"key":"2025043001414106400_ref54","doi-asserted-by":"publisher","first-page":"e799","DOI":"10.1371\/journal.pone.0000799","article-title":"Phage-antibiotic synergy (PAS): \u03b2-lactam and quinolone antibiotics stimulate virulent phage growth","volume":"2","author":"Comeau","year":"2007","journal-title":"PLoS One"},{"key":"2025043001414106400_ref55","doi-asserted-by":"publisher","first-page":"e5","DOI":"10.1016\/j.chom.2020.06.002","article-title":"The spatial heterogeneity of the gut limits predation and fosters coexistence of bacteria and bacteriophages","volume":"28","author":"Louren\u00e7o","year":"2020","journal-title":"Cell Host Microbe"},{"key":"2025043001414106400_ref56","doi-asserted-by":"publisher","first-page":"7971","DOI":"10.1038\/s41467-022-35351-w","article-title":"Multistep diversification in spatiotemporal bacterial-phage coevolution","volume":"13","author":"Shaer Tamar","year":"2022","journal-title":"Nat Commun"},{"key":"2025043001414106400_ref57","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1146\/annurev-phyto-080417-045858","article-title":"Multifaceted impacts of bacteriophages in the plant microbiome","volume":"56","author":"Koskella","year":"2018","journal-title":"Annu Rev Phytopathol"},{"key":"2025043001414106400_ref58","doi-asserted-by":"publisher","first-page":"fnv183","DOI":"10.1093\/femsle\/fnv183","article-title":"Revisiting bacterial cyclic nucleotide phosphodiesterases: cyclic AMP hydrolysis and beyond","volume":"362","author":"Matange","year":"2015","journal-title":"FEMS Microbiol Lett"},{"key":"2025043001414106400_ref59","doi-asserted-by":"publisher","first-page":"e01884","DOI":"10.1128\/mbio.01884-19","article-title":"Quorum sensing and metabolic state of the host control lysogeny-lysis switch of bacteriophage T1","volume":"10","author":"Laganenka","year":"2019","journal-title":"MBio"},{"key":"2025043001414106400_ref60","doi-asserted-by":"publisher","first-page":"e5","DOI":"10.1016\/j.chom.2022.03.014","article-title":"The gut environment regulates bacterial gene expression which modulates susceptibility to bacteriophage infection","volume":"30","author":"Louren\u00e7o","year":"2022","journal-title":"Cell Host Microbe"},{"key":"2025043001414106400_ref61","doi-asserted-by":"publisher","first-page":"e73679","DOI":"10.7554\/eLife.73679","article-title":"Parallel evolution of Pseudomonas aeruginosa phage resistance and virulence loss in response to phage treatment in vivo and in vitro","volume":"11","author":"Castledine","year":"2022","journal-title":"elife"},{"key":"2025043001414106400_ref62","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/j.cell.2022.11.017","article-title":"Phage therapy: from biological mechanisms to future directions","volume":"186","author":"Strathdee","year":"2023","journal-title":"Cell"},{"key":"2025043001414106400_ref63","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1146\/annurev-virology-091919-071712","article-title":"The social life of viruses","volume":"8","author":"Sanju\u00e1n","year":"2021","journal-title":"Annu Rev Virol"},{"key":"2025043001414106400_ref64","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1017\/CBO9780511541483.011","volume-title":"Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses","author":"Turner","year":"2008"},{"key":"2025043001414106400_ref65","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1134\/S0006297921030081","article-title":"Microbial arsenal of antiviral defenses\u2013part I","volume":"86","author":"Isaev","year":"2021","journal-title":"Biochemistry (Mosc)"},{"key":"2025043001414106400_ref66","doi-asserted-by":"publisher","first-page":"14341","DOI":"10.1038\/ncomms14341","article-title":"Cell fate decisions emerge as phages cooperate or compete inside their host","volume":"8","author":"Trinh","year":"2017","journal-title":"Nat Commun"},{"key":"2025043001414106400_ref67","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1126\/science.adl1356","article-title":"An intron endonuclease facilitates interference competition between coinfecting viruses","volume":"385","author":"Birkholz","year":"2024","journal-title":"Science"},{"key":"2025043001414106400_ref68","doi-asserted-by":"publisher","first-page":"2387","DOI":"10.1093\/molbev\/msu191","article-title":"Strength of selection pressure is an important parameter contributing to the complexity of antibiotic resistance evolution","volume":"31","author":"Oz","year":"2014","journal-title":"Mol Biol Evol"},{"key":"2025043001414106400_ref69","doi-asserted-by":"publisher","first-page":"3979","DOI":"10.1111\/1462-2920.14822","article-title":"Irregularities in genetic variation and mutation rates with environmental stresses","volume":"21","author":"Ferenci","year":"2019","journal-title":"Environ Microbiol"},{"key":"2025043001414106400_ref70","doi-asserted-by":"publisher","first-page":"e01652","DOI":"10.1128\/mbio.01652-19","article-title":"Resistance evolution against phage combinations depends on the timing and order of exposure","volume":"10","author":"Wright","year":"2019","journal-title":"MBio"},{"key":"2025043001414106400_ref71","doi-asserted-by":"publisher","first-page":"5646","DOI":"10.1128\/AEM.00757-12","article-title":"Effects of sequential and simultaneous applications of bacteriophages on populations of Pseudomonas aeruginosa in vitro and in wax moth larvae","volume":"78","author":"Hall","year":"2012","journal-title":"Appl Environ Microbiol"},{"key":"2025043001414106400_ref72","doi-asserted-by":"publisher","first-page":"e68876","DOI":"10.7554\/eLife.68876","article-title":"High potency of sequential therapy with only \u03b2-lactam antibiotics","volume":"10","author":"Batra","year":"2021","journal-title":"elife"},{"key":"2025043001414106400_ref73","doi-asserted-by":"publisher","first-page":"20220793","DOI":"10.1098\/rsif.2022.0793","article-title":"Sequential antibiotic therapy in the laboratory and in the patient","volume":"20","author":"Nyhoegen","year":"2023","journal-title":"J R Soc Interface"},{"key":"2025043001414106400_ref74","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1093\/emph\/eoz008","article-title":"Evolutionary ecology meets the antibiotic crisis: can we control pathogen adaptation through sequential therapy?","volume":"1","author":"Roemhild","year":"2019","journal-title":"Evol Med Public Health"},{"key":"2025043001414106400_ref75","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1038\/s41579-019-0201-x","article-title":"Pushing the envelope: LPS modifications and their consequences","volume":"17","author":"Simpson","year":"2019","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\/wraf065\/62874835\/wraf065.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ismej\/article-pdf\/19\/1\/wraf065\/62874835\/wraf065.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ismej\/article-pdf\/19\/1\/wraf065\/62874835\/wraf065.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,4,30]],"date-time":"2025-04-30T01:41:48Z","timestamp":1745977308000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ismej\/article\/doi\/10.1093\/ismejo\/wraf065\/8106832"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1]]},"references-count":75,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2025,1,2]]}},"URL":"https:\/\/doi.org\/10.1093\/ismejo\/wraf065","relation":{},"ISSN":["1751-7362","1751-7370"],"issn-type":[{"value":"1751-7362","type":"print"},{"value":"1751-7370","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,1]]},"published":{"date-parts":[[2025,1]]},"article-number":"wraf065"}}