{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T06:08:24Z","timestamp":1792822104441,"version":"4.5.0"},"reference-count":52,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,1,28]],"date-time":"2026-01-28T00:00:00Z","timestamp":1769558400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,2,19]],"date-time":"2026-02-19T00:00:00Z","timestamp":1771459200000},"content-version":"vor","delay-in-days":22,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100009367","name":"Mansoura University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100009367","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Ann Clin Microbiol Antimicrob"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>In this study, we were aimed to investigate the impact of co-cultures of different bacterial species on bacterial antibiotic resistance and virulence.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      The effect of co-cultures of\n                      <jats:italic>Pseudomonas aeruginosa<\/jats:italic>\n                      (Gram-negative bacteria) and\n                      <jats:italic>Staphylococcus aureus<\/jats:italic>\n                      (Gram-positive bacteria) on antibiotic resistance, virulence and biofilm formation in\n                      <jats:italic>P. aeruginosa<\/jats:italic>\n                      was examined in vitro in 14 mixtures. These mixtures were categorized into three groups: Standard category (including standard strains), naturally co-isolated category (co-isolated from the same patient) and random co-culture category (bacterial species from different patients). Additionally, the impact of the standard category on pathogenicity was assessed in vivo using mouse model. Intergroup comparisons were conducted using multiple\n                      <jats:italic>t<\/jats:italic>\n                      -test and comparisons between treated and untreated control isolates grown under the same conditions were made. Survival experiments were analyzed using Mantel-Cox log-rank test.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      <jats:italic>P. aeruginosa<\/jats:italic>\n                      survival significantly increased in most of the co-culture mixtures when treated with meropenem (92.9%), ceftazidime (85.7%), cefepime (78.6%), gentamicin (78.6%) and ciprofloxacin (71.4%). Similarly, virulence factor production significantly increased in\n                      <jats:italic>P. aeruginosa<\/jats:italic>\n                      in most of the investigated co-cultures as follows: pyocyanin (71.4%), elastase (71.4%), protease (78.6%), hemolysin (71.4%), lecithinase (78.6%), gelatinase (63.6%) and biofilm (71.4%). At the molecular level, the relative expression of the tested virulence-encoding genes;\n                      <jats:italic>pelA<\/jats:italic>\n                      ,\n                      <jats:italic>lasB<\/jats:italic>\n                      and\n                      <jats:italic>lasA<\/jats:italic>\n                      were significantly increased in at least 92.9% of the co-culture mixtures, especially in random ones, compared to their mono-culture, but with varying up-regulation degree (ranging from 1.5 to 96-fold increase).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>\n                      Finally, in vitro investigations for antibiotic resistance and virulence production clearly demonstrated a synergistic interaction between\n                      <jats:italic>P. aeruginosa<\/jats:italic>\n                      and\n                      <jats:italic>S. aureus<\/jats:italic>\n                      in the co-existence mixture. Compared to\n                      <jats:italic>P. aeruginosa<\/jats:italic>\n                      mono-cultures, the co-cultured strains exhibited enhanced resistance profiles and increased expression of key virulence factors, indicating that the simultaneous presence of both species promotes mutual adaptation and potentiation of pathogenic traits. Additionally, in vivo experiments confirmed that the co-infection with\n                      <jats:italic>S. aureus<\/jats:italic>\n                      significantly enhanced the pathogenicity of\n                      <jats:italic>P. aeruginosa<\/jats:italic>\n                      , as indicated by increased mortality rates and higher bacterial counts in lung tissues. Altogether, our results shed light on the impact of the co-existence of microbial species on bacterial virulence and antibiotic resistance.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12941-025-00843-2","type":"journal-article","created":{"date-parts":[[2026,1,28]],"date-time":"2026-01-28T11:16:48Z","timestamp":1769599008000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Coexistence with Staphylococcus aureus modulates the virulence and antibiotic resistance of Pseudomonas aeruginosa"],"prefix":"10.1186","volume":"25","author":[{"given":"Zeinab M.","family":"Helal","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Soha Lotfy","family":"Elshaer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohammed","family":"El-Mowafy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elsayed E.","family":"Habib","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,1,28]]},"reference":[{"key":"843_CR1","doi-asserted-by":"publisher","unstructured":"Anju VT, Busi S, Imchen M, Kumavath R, Mohan MS, Salim SA et al. Polymicrobial infections and biofilms: clinical significance and eradication strategies. Antibiot (Basel). 2022;11(12):1731. https:\/\/doi.org\/10.3390\/antibiotics11121731}","DOI":"10.3390\/antibiotics11121731"},{"key":"843_CR2","doi-asserted-by":"publisher","unstructured":"Nickol ME, Ciric J, Falcinelli SD, Chertow DS, Kindrachuk J. Characterization of host and bacterial contributions to lung barrier dysfunction following co-infection with 2009 pandemic influenza and methicillin resistant Staphylococcus aureus. Viruses. 2019;11(2):116. https:\/\/doi.org\/10.3390\/v11020116}","DOI":"10.3390\/v11020116"},{"key":"843_CR3","doi-asserted-by":"publisher","first-page":"104518","DOI":"10.1016\/j.meegid.2020.104518","volume":"85","author":"H Tahmasebi","year":"2020","unstructured":"Tahmasebi H, Dehbashi S, Arabestani MR. Co-harboring of mcr-1 and \u03b2-lactamase genes in Pseudomonas aeruginosa by high-resolution melting curve analysis (HRMA): molecular typing of Superbug strains in bloodstream infections (BSI). Infect Genet Evol. 2020;85:104518.","journal-title":"Infect Genet Evol"},{"issue":"4","key":"843_CR4","doi-asserted-by":"publisher","first-page":"e0097622","DOI":"10.1128\/spectrum.00976-22","volume":"10","author":"EE Bernardy","year":"2022","unstructured":"Bernardy EE, Raghuram V, Goldberg JB. Staphylococcus aureus and Pseudomonas aeruginosa isolates from the same cystic fibrosis respiratory sample coexist in coculture. Microbiol Spectr. 2022;10(4):e0097622.","journal-title":"Microbiol Spectr"},{"issue":"5","key":"843_CR5","doi-asserted-by":"publisher","first-page":"e0304491","DOI":"10.1371\/journal.pone.0304491","volume":"19","author":"PK Vestweber","year":"2024","unstructured":"Vestweber PK, W\u00e4chter J, Planz V, Jung N, Windbergs M. The interplay of Pseudomonas aeruginosa and Staphylococcus aureus in dual-species biofilms impacts development, antibiotic resistance and virulence of biofilms in in vitro wound infection models. PLoS ONE. 2024;19(5):e0304491.","journal-title":"PLoS ONE"},{"key":"843_CR6","doi-asserted-by":"publisher","first-page":"926758","DOI":"10.3389\/fcimb.2022.926758","volume":"12","author":"C Liao","year":"2022","unstructured":"Liao C, Huang X, Wang Q, Yao D, Lu W. Virulence factors of Pseudomonas aeruginosa and antivirulence strategies to combat its drug resistance. Front Cell Infect Microbiol. 2022;12:926758.","journal-title":"Front Cell Infect Microbiol"},{"key":"843_CR7","doi-asserted-by":"publisher","unstructured":"Jurado-Mart\u00edn I, Sainz-Mej\u00edas M, McClean S. Pseudomonas aeruginosa: an audacious pathogen with an adaptable arsenal of virulence factors. Int J Mol Sci. 2021;22(6):3128. } https:\/\/doi.org\/10.3390\/ijms22063128}","DOI":"10.3390\/ijms22063128"},{"key":"843_CR8","doi-asserted-by":"publisher","unstructured":"Sharma S, Mohler J, Mahajan SD, Schwartz SA, Bruggemann L, Aalinkeel R. Microbial biofilm: a review on formation, infection, antibiotic resistance, control measures, and innovative treatment. Microorganisms. 2023;11(6):1614. https:\/\/doi.org\/10.3390\/microorganisms11061614}","DOI":"10.3390\/microorganisms11061614"},{"key":"843_CR9","doi-asserted-by":"publisher","first-page":"101747","DOI":"10.1016\/j.cimid.2022.101747","volume":"81","author":"M Shahbandeh","year":"2022","unstructured":"Shahbandeh M, Moosazadeh Moghaddam M, Golmohammadi R, Mirnejad R. The antimicrobial effect of quorum sensing autoinducers of Pseudomonas aeruginosa, C12-HSL and C4-HSL, against MDR Staphylococcus aureus isolates. Comp Immunol Microbiol Infect Dis. 2022;81:101747.","journal-title":"Comp Immunol Microbiol Infect Dis"},{"issue":"51","key":"843_CR10","doi-asserted-by":"publisher","first-page":"e2212340119","DOI":"10.1073\/pnas.2212340119","volume":"119","author":"CB Ibberson","year":"2022","unstructured":"Ibberson CB, Barraza JP, Holmes AL, Cao P, Whiteley M. Precise Spatial structure impacts antimicrobial susceptibility of S. aureus in polymicrobial wound infections. Proc Natl Acad Sci U S A. 2022;119(51):e2212340119.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"843_CR11","doi-asserted-by":"publisher","first-page":"266","DOI":"10.3389\/fcimb.2020.00266","volume":"10","author":"P Briaud","year":"2020","unstructured":"Briaud P, Bastien S, Camus L, Boyadjian M, Reix P, Mainguy C, et al. Impact of coexistence phenotype between Staphylococcus aureus and Pseudomonas aeruginosa isolates on clinical outcomes among cystic fibrosis patients. Front Cell Infect Microbiol. 2020;10:266.","journal-title":"Front Cell Infect Microbiol"},{"key":"843_CR12","doi-asserted-by":"publisher","unstructured":"Ezeador C, Ejikeugwu C, Ushie S, Agbakoba N, Isolation. Identification and prevalence of Pseudomonas aeruginosa isolates from clinical and environmental sources in Onitsha Metropolis, Anambra state. Eur J Med Health Sci. 2020;2(2). } https:\/\/doi.org\/10.24018\/ejmed.2020.2.2.188}","DOI":"10.24018\/ejmed.2020.2.2.188"},{"issue":"4","key":"843_CR13","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1093\/ajcp\/45.4_ts.493","volume":"45","author":"AW Bauer","year":"1966","unstructured":"Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45(4):493\u20136.","journal-title":"Am J Clin Pathol"},{"key":"843_CR14","unstructured":"CLSI. Performance standards for antimicrobial susceptibility testing. Clinical and laboratory standard institute. 2021."},{"key":"843_CR15","doi-asserted-by":"publisher","first-page":"14849","DOI":"10.1038\/s41598-020-71834-w","volume":"10","author":"E Trizna","year":"2020","unstructured":"Trizna E, Yarullina M, Baidamshina D, Mironova A, Akhatova F, Rozhina E, et al. Bidirectional alterations in antibiotics susceptibility in Staphylococcus aureus-Pseudomonas aeruginosa dual-species biofilm. Sci Rep. 2020;10:14849.","journal-title":"Sci Rep"},{"issue":"1","key":"843_CR16","doi-asserted-by":"publisher","first-page":"9027","DOI":"10.1038\/s41598-022-12650-2","volume":"12","author":"MA Alford","year":"2022","unstructured":"Alford MA, Mann S, Akhoundsadegh N, Hancock REW. Competition between Pseudomonas aeruginosa and Staphylococcus aureus is dependent on intercellular signaling and regulated by the NtrBC two-component system. Sci Rep. 2022;12(1):9027.","journal-title":"Sci Rep"},{"issue":"1","key":"843_CR17","doi-asserted-by":"publisher","first-page":"16564","DOI":"10.1038\/s41598-019-52975-z","volume":"9","author":"P Briaud","year":"2019","unstructured":"Briaud P, Camus L, Bastien S, Dol\u00e9ans-Jordheim A, Vandenesch F, Moreau K. Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells. Sci Rep. 2019;9(1):16564.","journal-title":"Sci Rep"},{"issue":"2","key":"843_CR18","doi-asserted-by":"publisher","first-page":"884","DOI":"10.1128\/jb.172.2.884-900.1990","volume":"172","author":"DW Essar","year":"1990","unstructured":"Essar DW, Eberly L, Hadero A, Crawford IP. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol. 1990;172(2):884\u2013900.","journal-title":"J Bacteriol"},{"issue":"1","key":"843_CR19","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1007\/s12038-011-9011-7","volume":"36","author":"KS Musthafa","year":"2011","unstructured":"Musthafa KS, Saroja V, Pandian SK, Ravi AV. Antipathogenic potential of marine Bacillus sp. SS4 on N-acyl-homoserine-lactone-mediated virulence factors production in Pseudomonas aeruginosa (PAO1). J Biosci. 2011;36(1):55\u201367.","journal-title":"J Biosci"},{"key":"843_CR20","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1016\/j.micpath.2014.07.008","volume":"74","author":"SA El-Mowafy","year":"2014","unstructured":"El-Mowafy SA, Abd El Galil KH, El-Messery SM, Shaaban MI. Aspirin is an efficient inhibitor of quorum sensing, virulence and toxins in Pseudomonas aeruginosa. Microb Pathog. 2014;74:25\u201332.","journal-title":"Microb Pathog"},{"issue":"2","key":"843_CR21","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1016\/j.job.2012.03.002","volume":"54","author":"T Sato","year":"2012","unstructured":"Sato T, Kamaguchi A, Nakazawa F. Purification and characterization of hemolysin from prevotella Oris. J Oral Biosci. 2012;54(2):113\u20138.","journal-title":"J Oral Biosci"},{"key":"843_CR22","doi-asserted-by":"publisher","first-page":"687","DOI":"10.5897\/AJMR2016.8001","volume":"10","author":"S Hassan","year":"2016","unstructured":"Hassan S, Eid D. Effect of tyrosol on Staphylococcus aureus antimicrobial susceptibility, biofilm formation and virulence factors. Afr J Microbiol Res. 2016;10:687\u201393.","journal-title":"Afr J Microbiol Res"},{"issue":"3","key":"843_CR23","doi-asserted-by":"publisher","first-page":"208","DOI":"10.1016\/j.ijfoodmicro.2006.09.004","volume":"112","author":"F Lopes Mde","year":"2006","unstructured":"Lopes Mde F, Sim\u00f5es AP, Tenreiro R, Marques JJ, Crespo MT. Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int J Food Microbiol. 2006;112(3):208\u201314.","journal-title":"Int J Food Microbiol"},{"key":"843_CR24","doi-asserted-by":"publisher","first-page":"102580","DOI":"10.1016\/j.anaerobe.2022.102580","volume":"76","author":"C Abbott","year":"2022","unstructured":"Abbott C, Grout E, Morris T, Brown HL. Cutibacterium acnes biofilm forming clinical isolates modify the formation and structure of Staphylococcus aureus biofilms, increasing their susceptibility to antibiotics. Anaerobe. 2022;76:102580.","journal-title":"Anaerobe"},{"issue":"21","key":"843_CR25","doi-asserted-by":"publisher","first-page":"7223","DOI":"10.1007\/s00253-022-12144-1","volume":"106","author":"M Soliman","year":"2022","unstructured":"Soliman M, Said HS, El-Mowafy M, Barwa R, Novel. PCR detection of CRISPR\/Cas systems in Pseudomonas aeruginosa and its correlation with antibiotic resistance. Appl Microbiol Biotechnol. 2022;106(21):7223\u201334.","journal-title":"Appl Microbiol Biotechnol"},{"key":"843_CR26","doi-asserted-by":"publisher","unstructured":"Limoli DH, Whitfield GB, Kitao T, Ivey ML, Davis MR Jr., Grahl N et al. Pseudomonas aeruginosa alginate overproduction promotes coexistence with Staphylococcus aureus in a model of cystic fibrosis respiratory infection. mBio. 2017;8(2):e00186-17. https:\/\/doi.org\/10.1128\/mBio.00186-17}","DOI":"10.1128\/mBio.00186-17"},{"issue":"4","key":"843_CR27","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","volume":"25","author":"KJ Livak","year":"2001","unstructured":"Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta delta C(T)) method. Methods. 2001;25(4):402\u20138.","journal-title":"Methods"},{"issue":"10","key":"843_CR28","doi-asserted-by":"publisher","first-page":"1194","DOI":"10.1099\/jmm.0.000327","volume":"65","author":"S El-Shaer","year":"2016","unstructured":"El-Shaer S, Shaaban M, Barwa R, Hassan R. Control of quorum sensing and virulence factors of Pseudomonas aeruginosa using phenylalanine arginyl \u03b2-naphthylamide. J Med Microbiol. 2016;65(10):1194\u2013204.","journal-title":"J Med Microbiol"},{"issue":"1","key":"843_CR29","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1007\/s10989-019-09841-3","volume":"26","author":"M Meskini","year":"2020","unstructured":"Meskini M, Ghorbani M, Bahadoran H, zaree A, Esmaeili D. ZOUSH ointment with the properties of antibacterial Moreover, burn wound healing. Int J Pept Res Ther. 2020;26(1):349\u201355.","journal-title":"Int J Pept Res Ther"},{"issue":"4","key":"843_CR30","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1161\/CIRCRESAHA.109.195230","volume":"105","author":"K Li","year":"2009","unstructured":"Li K, Xu W, Guo Q, Jiang Z, Wang P, Yue Y, et al. Differential macrophage polarization in male and female BALB\/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circ Res. 2009;105(4):353\u201364.","journal-title":"Circ Res"},{"key":"843_CR31","doi-asserted-by":"publisher","unstructured":"Alonaizan R, Woods S, Hargrave KE, Roberts CW. An exaggerated immune response in female BALB\/c mice controls initial Toxoplasma gondii multiplication but increases mortality and morbidity relative to male mice. Pathogens. 2021;10(9):1154. https:\/\/doi.org\/10.3390\/pathogens10091154}","DOI":"10.3390\/pathogens10091154"},{"issue":"1","key":"843_CR32","doi-asserted-by":"publisher","first-page":"132","DOI":"10.30802\/AALAS-JAALAS-24-075","volume":"64","author":"S Patel","year":"2025","unstructured":"Patel S, Patel S, Kotadiya A, Patel S, Shrimali B, Tank M, et al. Comparative analysis of the effect of sex and age on the hematological and biochemical profile of BALB\/c and C57BL\/6 inbred mice. J Am Assoc Lab Anim Sci. 2025;64(1):132\u201345.","journal-title":"J Am Assoc Lab Anim Sci"},{"issue":"6","key":"843_CR33","doi-asserted-by":"publisher","first-page":"446","DOI":"10.30802\/AALAS-CM-22-000124","volume":"73","author":"LT Ferguson","year":"2023","unstructured":"Ferguson LT, Rashied AA, Liang Z, Yumoto T, Anyalebechi JC, Swift DA, et al. A novel scoring system for humane endpoints in mice with cecal ligation and Puncture-Induced sepsis. Comp Med. 2023;73(6):446\u201360.","journal-title":"Comp Med"},{"issue":"6","key":"843_CR34","doi-asserted-by":"publisher","first-page":"933","DOI":"10.1093\/infdis\/jix621","volume":"217","author":"C Cigana","year":"2018","unstructured":"Cigana C, Bianconi I, Baldan R, De Simone M, Riva C, Sipione B, et al. Staphylococcus aureus impacts Pseudomonas aeruginosa chronic respiratory disease in murine models. J Infect Dis. 2018;217(6):933\u201342.","journal-title":"J Infect Dis"},{"key":"843_CR35","doi-asserted-by":"publisher","first-page":"2880","DOI":"10.3389\/fmicb.2019.02880","volume":"10","author":"G Millette","year":"2019","unstructured":"Millette G, Langlois JP, Brouillette E, Frost EH, Cantin AM, Malouin F. Despite antagonism in vitro, Pseudomonas aeruginosa enhances Staphylococcus aureus colonization in a murine lung infection model. Front Microbiol. 2019;10:2880.","journal-title":"Front Microbiol"},{"key":"843_CR36","doi-asserted-by":"publisher","first-page":"811474","DOI":"10.3389\/fcimb.2022.811474","volume":"12","author":"EC Peres-Emidio","year":"2022","unstructured":"Peres-Emidio EC, Freitas GJC, Costa MC, Gouveia-Eufrasio L, Silva LMV, Santos APN, et al. Pseudomonas aeruginosa infection modulates the immune response and increases mice resistance to Cryptococcus Gattii. Front Cell Infect Microbiol. 2022;12:811474.","journal-title":"Front Cell Infect Microbiol"},{"key":"843_CR37","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1186\/1756-0500-7-233","volume":"7","author":"B Shrum","year":"2014","unstructured":"Shrum B, Anantha RV, Xu SX, Donnelly M, Haeryfar SM, McCormick JK, et al. A robust scoring system to evaluate sepsis severity in an animal model. BMC Res Notes. 2014;7:233.","journal-title":"BMC Res Notes"},{"issue":"1","key":"843_CR38","doi-asserted-by":"publisher","first-page":"2186331","DOI":"10.1080\/21505594.2023.2186331","volume":"14","author":"RS Dudis","year":"2023","unstructured":"Dudis RS, Wong TY, Escatte MG, Alamneh YA, Abu-Taleb R, Su W, et al. Longitudinal temperature measurement can determine humane endpoints in BALB\/c mouse models of ESKAPEE infection. Virulence. 2023;14(1):2186331.","journal-title":"Virulence"},{"issue":"26","key":"843_CR39","doi-asserted-by":"publisher","first-page":"3387","DOI":"10.1016\/j.vaccine.2017.05.017","volume":"35","author":"S Ainsworth","year":"2017","unstructured":"Ainsworth S, Ketter PM, Yu JJ, Grimm RC, May HC, Cap AP, et al. Vaccination with a live attenuated acinetobacter baumannii deficient in thioredoxin provides protection against systemic acinetobacter infection. Vaccine. 2017;35(26):3387\u201394.","journal-title":"Vaccine"},{"key":"843_CR40","doi-asserted-by":"publisher","unstructured":"Armbruster CR, Wolter DJ, Mishra M, Hayden HS, Radey MC, Merrihew G et al. Staphylococcus aureus protein A mediates interspecies interactions at the cell surface of Pseudomonas aeruginosa. mBio. 2016;7(3):e00538-16. https:\/\/doi.org\/10.1128\/mBio.00538-16}","DOI":"10.1128\/mBio.00538-16"},{"issue":"1","key":"843_CR41","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1186\/s13568-021-01210-y","volume":"11","author":"S Dehbashi","year":"2021","unstructured":"Dehbashi S, Alikhani MY, Tahmasebi H, Arabestani MR. The inhibitory effects of Staphylococcus aureus on the antibiotic susceptibility and virulence factors of Pseudomonas aeruginosa: A549 cell line model. AMB Express. 2021;11(1):50.","journal-title":"AMB Express"},{"issue":"1","key":"843_CR42","doi-asserted-by":"publisher","first-page":"16284","DOI":"10.1038\/s41598-019-52726-0","volume":"9","author":"MDM Cendra","year":"2019","unstructured":"Cendra MDM, Blanco-Cabra N, Pedraz L, Torrents E. Optimal environmental and culture conditions allow the in vitro coexistence of Pseudomonas aeruginosa and Staphylococcus aureus in stable biofilms. Sci Rep. 2019;9(1):16284.","journal-title":"Sci Rep"},{"key":"843_CR43","doi-asserted-by":"publisher","unstructured":"Barraza JP, Whiteley M. A Pseudomonas aeruginosa antimicrobial affects the biogeography but not fitness of Staphylococcus aureus during coculture. mBio. 2021;12(2):e00047-21. https:\/\/doi.org\/10.1128\/mBio.00047-21}","DOI":"10.1128\/mBio.00047-21"},{"issue":"1","key":"843_CR44","doi-asserted-by":"publisher","first-page":"1092","DOI":"10.1186\/s12879-024-10001-2","volume":"24","author":"H Luo","year":"2024","unstructured":"Luo H, Ni L, Chen T, Huang L, Zhang X, Li X, et al. Intraspecific Cooperation allows the survival of Staphylococcus aureus staff: a novel strategy for disease relapse. BMC Infect Dis. 2024;24(1):1092.","journal-title":"BMC Infect Dis"},{"key":"843_CR45","doi-asserted-by":"publisher","first-page":"112540","DOI":"10.1016\/j.celrep.2023.112540","volume":"42","author":"C Jenul","year":"2023","unstructured":"Jenul C, Keim K, Jens J, Zeiler M, Schilcher K, Schurr M, et al. Pyochelin biotransformation by Staphylococcusaureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infections. Cell Rep. 2023;42:112540.","journal-title":"Cell Rep"},{"issue":"5","key":"843_CR46","doi-asserted-by":"publisher","first-page":"641","DOI":"10.1016\/j.chom.2019.03.006","volume":"25","author":"LR Kalan","year":"2019","unstructured":"Kalan LR, Meisel JS, Loesche MA, Horwinski J, Soaita I, Chen X, et al. Strain-and species-level variation in the Microbiome of diabetic wounds is associated with clinical outcomes and therapeutic efficacy. Cell Host Microbe. 2019;25(5):641\u201355. e5.","journal-title":"Cell Host Microbe"},{"key":"843_CR47","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1038\/s41522-017-0035-0","volume":"3","author":"T Beaudoin","year":"2017","unstructured":"Beaudoin T, Yau YCW, Stapleton PJ, Gong Y, Wang PW, Guttman DS, et al. Staphylococcus aureus interaction with Pseudomonas aeruginosa biofilm enhances tobramycin resistance. NPJ Biofilms Microbiomes. 2017;3:25.","journal-title":"NPJ Biofilms Microbiomes"},{"key":"843_CR48","doi-asserted-by":"publisher","first-page":"824042","DOI":"10.3389\/fcimb.2021.824042","volume":"11","author":"L Biswas","year":"2021","unstructured":"Biswas L, G\u00f6tz F. Molecular mechanisms of Staphylococcus and Pseudomonas interactions in cystic fibrosis. Front Cell Infect Microbiol. 2021;11:824042.","journal-title":"Front Cell Infect Microbiol"},{"key":"843_CR49","doi-asserted-by":"publisher","first-page":"106","DOI":"10.3389\/fcimb.2017.00106","volume":"7","author":"A Hotterbeekx","year":"2017","unstructured":"Hotterbeekx A, Kumar-Singh S, Goossens H, Malhotra-Kumar S. In vivo and in vitro interactions between Pseudomonas aeruginosa and Staphylococcus spp. Front Cell Infect Microbiol. 2017;7:106.","journal-title":"Front Cell Infect Microbiol"},{"key":"843_CR50","doi-asserted-by":"publisher","unstructured":"Alves PM, Al-Badi E, Withycombe C, Jones PM, Purdy KJ, Maddocks SE. Interaction between Staphylococcus aureus and Pseudomonas aeruginosa is beneficial for colonisation and pathogenicity in a mixed biofilm. Pathog Dis. 2018;76(1):10.1093\/femspd\/fty003. } } https:\/\/doi.org\/10.1093\/femspd\/fty003}","DOI":"10.1093\/femspd\/fty003"},{"issue":"1","key":"843_CR51","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1186\/s12864-018-5398-y","volume":"20","author":"M Tognon","year":"2019","unstructured":"Tognon M, K\u00f6hler T, Luscher A, van Delden C. Transcriptional profiling of Pseudomonas aeruginosa and Staphylococcus aureus during in vitro co-culture. BMC Genomics. 2019;20(1):30.","journal-title":"BMC Genomics"},{"issue":"6","key":"843_CR52","doi-asserted-by":"publisher","first-page":"1820","DOI":"10.1111\/jam.14598","volume":"128","author":"G Silva-Santana","year":"2020","unstructured":"Silva-Santana G, Aguiar-Alves F, Lenzi-Almeida KC, Lopes VGS, Silva LE, Hirata J\u00fanior R, et al. Pathological profiles of systemic infections by Panton-Valentine leukocidin-positive, methicillin-resistant Staphylococcus aureus strains in a murine model. J Appl Microbiol. 2020;128(6):1820\u201342.","journal-title":"J Appl Microbiol"}],"container-title":["Annals of Clinical Microbiology and Antimicrobials"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12941-025-00843-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12941-025-00843-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12941-025-00843-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,2,20]],"date-time":"2026-02-20T00:04:49Z","timestamp":1771545889000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1186\/s12941-025-00843-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1,28]]},"references-count":52,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["843"],"URL":"https:\/\/doi.org\/10.1186\/s12941-025-00843-2","relation":{},"ISSN":["1476-0711"],"issn-type":[{"value":"1476-0711","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,28]]},"assertion":[{"value":"18 August 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 December 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 January 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All specimens were obtained from different Mansoura University Hospitals and Clinics after approval from the ethical research committee, Faculty of Pharmacy, Mansoura University, following the medical research requirements in the usage, handling and care of human subjects (Ethical code:2025-97.). Informed consent was obtained from patients from whom the clinical specimens were obtained in this work. Regarding in vivo experiments in mice, all procedures, care and handling of the animals were performed according to institutional and national ethical guidelines. Additionally, the study was approved by the Animal Care and Use Committee, Mansoura University (MU-ACUC (PHARM.PHD.24.05.41).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Informed consents were obtained from patients from whom the clinical specimens were obtained in this work.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"14"}}