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Resistance evolution can disrupt antibiotic exposure protection through competitive exclusion of the protective species

  • Laxminarayan R, Duse A, Wattal C, Zaidi AKM, Wertheim HFL, Sumpradit N, et al. Antibiotic resistance—the need for global solutions. Lancet Infect Dis. 2013;13:1057–98.

    PubMed 
    Article 

    Google Scholar 

  • Murray CJ, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399:629–55.

    CAS 
    Article 

    Google Scholar 

  • O’Neil J. Antimicrobial resistance: tackling a crisis for the health and wealth of nations. The review on antimicrobial resistance. 2014. https://amr-review.org/sites/default/files/AMRReviewPaper-Tacklingacrisisforthehealthandwealthofnations_1.pdf.

  • Pang Z, Raudonis R, Glick BR, Lin T-J, Cheng Z. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and alternative therapeutic strategies. Biotechnol Adv. 2019;37:177–92.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Vandeplassche E, Tavernier S, Coenye T, Crabbé A. Influence of the lung microbiome on antibiotic susceptibility of cystic fibrosis pathogens. Eur Respir Rev. 2019;28:190041.

    PubMed 
    Article 

    Google Scholar 

  • Wheatley R, Diaz Caballero J, Kapel N, de Winter FHR, Jangir P, Quinn A, et al. Rapid evolution and host immunity drive the rise and fall of carbapenem resistance during an acute Pseudomonas aeruginosa infection. Nat Commun. 2021;12:2460.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Adamowicz EM, Flynn J, Hunter RC, Harcombe WR. Cross-feeding modulates antibiotic tolerance in bacterial communities. ISME J. 2018;12:2723–35.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Allison DG, Matthews MJ. Effect of polysaccharide interactions on antibiotic susceptibility of Pseudomonas aeruginosa. J Appl Bacteriol. 1992;73:484–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Beaudoin T, Yau YCW, Stapleton PJ, Gong Y, Wang PW, Guttman DS, et al. Staphylococcus aureus with Pseudomonas aeruginosa biofilm enhances tobramycin resistance. Npj Biofilms Microbiomes. 2017;3:25.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bottery MJ, Matthews JL, Wood AJ, Johansen HK, Pitchford JW, Friman V-P. Inter-species interactions alter antibiotic efficacy in bacterial communities. ISME J. 2022;16:812–21.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Elias S, Banin E. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 2012;36:990–1004.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hoffman LR, Deziel E, D’Argenio DA, Lepine F, Emerson J, McNamara S, et al. Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 2006;103:19890–5.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Molina-Santiago C, Daddaoua A, Fillet S, Duque E, Ramos J-L. Interspecies signalling: Pseudomonas putida efflux pump TtgGHI is activated by indole to increase antibiotic resistance: Antibiotic resistance. Environ Microbiol. 2014;16:1267–81.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Orazi G, O’Toole GA. Pseudomonas aeruginosa alters Staphylococcus aureus sensitivity to vancomycin in a biofilm model of cystic fibrosis infection. mBio. 2017;8:e00873–17. https://doi.org/10.1128/mBio.00873-17.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Perlin MH, Clark DR, McKenzie C, Patel H, Jackson N, Kormanik C, et al. Protection of Salmonella by ampicillin-resistant Escherichia coli in the presence of otherwise lethal drug concentrations. Proc R Soc B Biol Sci. 2009;276:3759–68.

    CAS 
    Article 

    Google Scholar 

  • Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, et al. Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol. 2008;68:75–86.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Sherrard LJ, McGrath SJ, McIlreavey L, Hatch J, Wolfgang MC, Muhlebach MS, et al. Production of extended-spectrum β -lactamases and the potential indirect pathogenic role of Prevotella isolates from the cystic fibrosis respiratory microbiota. Int J Antimicrob Agents. 2016;47:140–5.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Tognon M, Köhler T, Gdaniec BG, Hao Y, Lam JS, Beaume M, et al. Co-evolution with Staphylococcus aureus leads to lipopolysaccharide alterations in Pseudomonas aeruginosa. ISME J. 2017;11:2233–43.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Adamowicz EM, Muza M, Chacón JM, Harcombe WR. Cross-feeding modulates the rate and mechanism of antibiotic resistance evolution in a model microbial community of Escherichia coli and Salmonella enterica. PLOS Pathog. 2020;16:e1008700.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bottery MJ, Pitchford JW, Friman V-P. Ecology and evolution of antimicrobial resistance in bacterial communities. ISME J. 2021;15:939–48.

    PubMed 
    Article 

    Google Scholar 

  • Estrela S, Brown SP. Community interactions and spatial structure shape selection on antibiotic resistant lineages. PLOS Comput Biol. 2018;14:e1006179.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Klümper U, Recker M, Zhang L, Yin X, Zhang T, Buckling A, et al. Selection for antimicrobial resistance is reduced when embedded in a natural microbial community. ISME J. 2019;13:2927–37.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Scheuerl T, Hopkins M, Nowell RW, Rivett DW, Barraclough TG, Bell T. Bacterial adaptation is constrained in complex communities. Nat Commun. 2020;11:754.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Sorg RA, Lin L, van Doorn GS, Sorg M, Olson J, Nizet V, et al. Collective resistance in microbial communities by intracellular antibiotic deactivation. PLOS Biol. 2016;14:e2000631.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Kulczycki LL, Kostuch M, Bellanti JA. A clinical perspective of cystic fibrosis and new genetic findings: relationship of CFTR mutations to genotype-phenotype manifestations. Am J Med Genet. 2003;116A:262–7.

    PubMed 
    Article 

    Google Scholar 

  • Flume PA, Mogayzel PJ, Robinson KA, Rosenblatt RL, Quittell L, Marshall BC. Cystic fibrosis pulmonary guidelines: pulmonary complications: hemoptysis and pneumothorax. Am J Respir Crit Care Med. 2010;182:298–306.

    PubMed 
    Article 

    Google Scholar 

  • Belkin RA, Henig NR, Singer LG, Chaparro C, Rubenstein RC, Xie SX, et al. Risk factors for death of patients with cystic fibrosis awaiting lung transplantation. Am J Respir Crit Care Med. 2006;173:659–66.

    PubMed 
    Article 

    Google Scholar 

  • Martin C, Hamard C, Kanaan R, Boussaud V, Grenet D, Abély M, et al. Causes of death in French cystic fibrosis patients: the need for improvement in transplantation referral strategies! J Cyst Fibros. 2016;15:204–12.

    PubMed 
    Article 

    Google Scholar 

  • Döring G, Conway SP, Heijerman HGM, Hodson ME, Høiby N, Smyth A, et al. Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus. Eur Respir J. 2000;16:749.

    PubMed 
    Article 

    Google Scholar 

  • Marshall B, Faro A, Brown W, Elbert A, Fink A, Cromwell E, et al. Patient registry, annual data report. Bethesda, Maryland: Cystic Fibrosis Foundation; 2020. https://www.cff.org/sites/default/files/2021-11/Patient-Registry-Annual-Data-Report.pdf.

  • Vongthilath R, Richaud Thiriez B, Dehillotte C, Lemonnier L, Guillien A, Degano B, et al. Clinical and microbiological characteristics of cystic fibrosis adults never colonized by Pseudomonas aeruginosa: analysis of the French CF registry. PLOS ONE. 2019;14:e0210201.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Zolin A, Orenti A, Jung A, van Rens J. ECFSPR annual report 2019. Denmark: European Cystic Fibrosis Society Patient Registry; 2021. https://www.ecfs.eu/sites/default/files/general-content-files/working-groups/ecfs-patient-registry/ECFSPR_Report_2019_v1_16Feb2022.pdf.

  • Conrad D, Haynes M, Salamon P, Rainey PB, Youle M, Rohwer F. Cystic fibrosis therapy: a community ecology perspective. Am J Respir Cell Mol Biol. 2013;48:150–6.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Filkins LM, Graber JA, Olson DG, Dolben EL, Lynd LR, Bhuju S, et al. Coculture of Staphylococcus aureus with Pseudomonas aeruginosa drives S. aureus towards fermentative metabolism and reduced viability in a cystic fibrosis model. J Bacteriol. 2015;197:2252–64.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Zhao J, Schloss PD, Kalikin LM, Carmody LA, Foster BK, Petrosino JF, et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci USA. 2012;109:5809–14.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ballestero S, Vírseda I, Escobar H, Suárez L, Baquero F. Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis. 1995;14:728–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gladman G, Connor PJ, Williams RF, David TJ. Controlled study of Pseudomonas cepacia and Pseudomonas maltophilia in cystic fibrosis. Arch Dis Child. 1992;67:192–5.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Goss CH. Association between Stenotrophomonas maltophilia and lung function in cystic fibrosis. Thorax. 2004;59:955–9.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Parkins MD, Floto RA. Emerging bacterial pathogens and changing concepts of bacterial pathogenesis in cystic fibrosis. J Cyst Fibros. 2015;14:293–304.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Goss CH, Otto K, Aitken ML, Rubenfeld GD. Detecting Stenotrophomonas maltophilia does not reduce survival of patients with cystic fibrosis. Am J Respir Crit Care Med. 2002;166:356–61.

    PubMed 
    Article 

    Google Scholar 

  • Alonso A, Martínez JL. Multiple antibiotic resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother. 1997;41:1140–2.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Zhang L, Li XZ, Poole K. Multiple antibiotic resistance in Stenotrophomonas maltophilia: involvement of a multidrug efflux system. Antimicrob Agents Chemother. 2000;44:287–93.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Abda EM, Krysciak D, Krohn-Molt I, Mamat U, Schmeisser C, Förstner KU, et al. Phenotypic heterogeneity affects Stenotrophomonas maltophilia K279a colony morphotypes and β-lactamase expression. Front Microbiol. 2015;6:1373.

  • Okazaki A, Avison MB. Induction of L1 and L2 β-lactamase production in Stenotrophomonas maltophilia is dependent on an AmpR-type regulator. Antimicrob Agents Chemother. 2008;52:1525–8.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Walsh TR, Hall L, Assinder SJ, Nichols WW, Cartwright SJ, MacGowan AP, et al. Sequence analysis of the L1 metallo-β-lactamase from Xanthomonas maltophilia. Biochim Biophys Acta. 1994;1218:199–201.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Yang Z, Liu W, Cui Q, Niu W, Li H, Zhao X, et al. Prevalence and detection of Stenotrophomonas maltophilia carrying metallo-I2-lactamase blaL1 in Beijing, China. Front Microbiol. 2014;5:692.

  • Kataoka D, Fujiwara H, Kawakami T, Tanaka Y, Tanimoto A, Ikawa S, et al. The indirect pathogenicity of Stenotrophomonas maltophilia. Int J Antimicrob Agents. 2003;22:601–6.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Winstanley C, O’Brien S, Brockhurst MA. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol. 2016;24:327–37.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • McGuigan L, Callaghan M. The evolving dynamics of the microbial community in the cystic fibrosis lung. Environ Microbiol. 2015;17:16–28.

    PubMed 
    Article 

    Google Scholar 

  • Wistrand-Yuen E, Knopp M, Hjort K, Koskiniemi S, Berg OG, Andersson DI. Evolution of high-level resistance during low-level antibiotic exposure. Nat Commun. 2018;9:1599.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Mahrt N, Tietze A, Künzel S, Franzenburg S, Barbosa C, Jansen G, et al. Bottleneck size and selection level reproducibly impact evolution of antibiotic resistance. Nat Ecol Evol. 2021;5:1233–1242.

  • Govaert L, Altermatt F, De Meester L, Leibold MA, McPeek MA, Pantel JH, et al. Integrating fundamental processes to understand eco‐evolutionary community dynamics and patterns. Funct Ecol. 2021;35:2138–55.

    Article 

    Google Scholar 

  • Palmer KL, Aye LM, Whiteley M. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol. 2007;189:8079–87.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Souza Barbosa F, Capra Pezzi L, Tsao M, Oliveira TF, Manoela Dias Macedo S, Schapoval EES, et al. Stability and degradation products of imipenem applying High‐Resolution Mass Spectrometry: an analytical study focused on solutions for infusion. Biomed Chromatogr. 2018;33:4471.

  • Verpooten G, Verbist L, Buntinx A, Entwistle L, Jones K, Broe M. The pharmacokinetics of imipenem (thienamycin-formamidine) and the renal dehydropeptidase inhibitor cilastatin sodium in normal subjects and patients with renal failure. Br J Clin Pharmacol. 1984;18:183–93.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Li H, Luo Y-F, Williams BJ, Blackwell TS, Xie C-M. Structure and function of OprD protein in Pseudomonas aeruginosa: from antibiotic resistance to novel therapies. Int J Med Microbiol. 2012;302:63–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kousser C, Clark C, Sherrington S, Voelz K, Hall RA. Pseudomonas aeruginosa inhibits Rhizopus microsporus germination through sequestration of free environmental iron. Sci Rep. 2019;9:5714.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Schalk IJ, Guillon L. Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis: pyoverdine biosynthesis. Environ Microbiol. 2013;15:1661–73.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Duan X, Pan Y, Cai Z, Liu Y, Zhang Y, Liu M, et al. rpoS-mutation variants are selected in Pseudomonas aeruginosa biofilms under imipenem pressure. Cell Biosci. 2021;11:138.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Zhu K, Chen S, Sysoeva TA, You L. Universal antibiotic tolerance arising from antibiotic-triggered accumulation of pyocyanin in Pseudomonas aeruginosa. PLOS Biol. 2019;17:e3000573.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • El-Fouly MZ, Sharaf AM, Shahin AAM, El-Bialy HA, Omara AMA. Biosynthesis of pyocyanin pigment by Pseudomonas aeruginosa. J Radiat Res Appl Sci. 2015;8:36–48.

    CAS 
    Article 

    Google Scholar 

  • Baron SS, Rowe JJ. Antibiotic action of pyocyanin. Antimicrob Agents Chemother. 1981;20:814–20.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Kimura M, Ohta T. The average number of generations until fixation of a mutant gene in a finite population. Genetics. 1969;61:763–71.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Meirelles LA, Perry EK, Bergkessel M, Newman DK. Bacterial defenses against a natural antibiotic promote collateral resilience to clinical antibiotics. PLOS Biol. 2021;19:e3001093.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Hall JPJ, Harrison E, Brockhurst MA. Competitive species interactions constrain abiotic adaptation in a bacterial soil community. Evol Lett. 2018;2:580–9.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Scanlan PD, Hall AR, Blackshields G, Friman V-P, Davis MR, Goldberg JB, et al. Coevolution with bacteriophages drives genome-wide host evolution and constrains the acquisition of abiotic-beneficial mutations. Mol Biol Evol. 2015;32:1425–35.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Finkel SE. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat Rev Microbiol. 2006;4:113–20.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gefen O, Fridman O, Ronin I, Balaban NQ. Direct observation of single stationary-phase bacteria reveals a surprisingly long period of constant protein production activity. Proc Natl Acad Sci. 2014;111:556–61.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Fang Z, Zhang L, Huang Y, Qing Y, Cao K, Tian G, et al. OprD mutations and inactivation in imipenem-resistant Pseudomonas aeruginosa isolates from China. Infect Genet Evol. 2014;21:124–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hirabayashi A, Kato D, Tomita Y, Iguchi M, Yamada K, Kouyama Y, et al. Risk factors for and role of OprD protein in increasing minimal inhibitory concentrations of carbapenems in clinical isolates of Pseudomonas aeruginosa. J Med Microbiol. 2017;66:1562–72.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Huang H, Jeanteur D, Pattus F, Hancock REW. Membrane topology and site-specific mutagenesis of Pseudomonas aeruginosa porin OprD. Mol Microbiol. 1995;16:931–41.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Fournier D, Richardot C, Müller E, Robert-Nicoud M, Llanes C, Plésiat P, et al. Complexity of resistance mechanisms to imipenem in intensive care unit strains of Pseudomonas aeruginosa. J Antimicrob Chemother. 2013;68:1772–80.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kao C-Y, Chen S-S, Hung K-H, Wu H-M, Hsueh P-R, Yan J-J, et al. Overproduction of active efflux pump and variations of OprD dominate in imipenem-resistant Pseudomonas aeruginosa isolated from patients with bloodstream infections in Taiwan. BMC Microbiol. 2016;16:107.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Ocampo-Sosa AA, Cabot G, Rodríguez C, Roman E, Tubau F, Macia MD, et al. Alterations of OprD in carbapenem-intermediate and -susceptible strains of Pseudomonas aeruginosa isolated from patients with bacteremia in a Spanish multicenter study. Antimicrob Agents Chemother. 2012;56:1703–13.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Shu J-C, Kuo A-J, Su L-H, Liu T-P, Lee M-H, Su I-N, et al. Development of carbapenem resistance in Pseudomonas aeruginosa is associated with OprD polymorphisms, particularly the amino acid substitution at codon 170. J Antimicrob Chemother. 2017;72:2489–95.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Pernet E, Guillemot L, Burgel P-R, Martin C, Lambeau G, Sermet-Gaudelus I, et al. Pseudomonas aeruginosa eradicates Staphylococcus aureus by manipulating the host immunity. Nat Commun. 2014;5:5105.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Briaud P, Camus L, Bastien S, Doléans-Jordheim A, Vandenesch F, Moreau K. Coexistence with Pseudomonas aeruginosa alters Staphylococcus aureus transcriptome, antibiotic resistance and internalization into epithelial cells. Sci Rep. 2019;9:16564.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Khare A, Tavazoie S. Multifactorial competition and resistance in a two-species bacterial system. PLOS Genet. 2015;11:e1005715.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Mashburn LM, Jett AM, Akins DR, Whiteley M. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J Bacteriol. 2005;187:554–66.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Cirz RT, O’Neill BM, Hammond JA, Head SR, Romesberg FE. Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J Bacteriol. 2006;188:7101–10.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • García-Contreras R, Nuñez-López L, Jasso-Chávez R, Kwan BW, Belmont JA, Rangel-Vega A, et al. Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating. ISME J. 2015;9:115–25.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Moradali MF, Ghods S, Rehm BHA. Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 2017;7:39.

  • Vogt SL, Green C, Stevens KM, Day B, Erickson DL, Woods DE, et al. The stringent response is essential for Pseudomonas aeruginosa virulence in the rat lung agar bead and Drosophila melanogaster feeding models of infection. Infect Immun. 2011;79:4094–104.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Baron SS, Terranova G, Rowe JJ. Molecular mechanism of the antimicrobial action of pyocyanin. Curr Microbiol. 1989;18:223–30.

    CAS 
    Article 

    Google Scholar 

  • Castañeda-Tamez P, Ramírez-Peris J, Pérez-Velázquez J, Kuttler C, Jalalimanesh A, Saucedo-Mora MÁ, et al. Pyocyanin restricts social cheating in Pseudomonas aeruginosa. Front Microbiol. 2018;9:1348.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Fontoura R, Spada JC, Silveira ST, Tsai SM, Brandelli A. Purification and characterization of an antimicrobial peptide produced by Pseudomonas sp. strain 4B. World J Microbiol Biotechnol. 2009;25:205–13.

    CAS 
    Article 

    Google Scholar 

  • Hassan HM, Fridovich I. Mechanism of the antibiotic action pyocyanine. J Bacteriol. 1980;141:156–63.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Machan ZA, Pitt TL, White W, Watson D, Taylor GW, Cole PJ, et al. Interaction between Pseudomonas aeruginosa and Staphylococcus aureus: description of an antistaphylococcal substance. J Med Microbiol. 1991;34:213–7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Raji El Feghali PA, Nawas T. Pyocyanin: a powerful inhibitor of bacterial growth and biofilm formation. Madridge J Case Rep Stud. 2018;3:101–7.

    Article 

    Google Scholar 

  • Saha S, Thavasi R, Jayalakshmi S. Phenazine pigments from Pseudomonas aeruginosa and their application as antibacterial agent and food colourants. Res J Microbiol. 2008;3:122–8.

    CAS 
    Article 

    Google Scholar 

  • Schiessl KT, Hu F, Jo J, Nazia SZ, Wang B, Price-Whelan A, et al. Phenazine production promotes antibiotic tolerance and metabolic heterogeneity in Pseudomonas aeruginosa biofilms. Nat Commun. 2019;10:762.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Jagmann N, Brachvogel H-P, Philipp B. Parasitic growth of Pseudomonas aeruginosa in co-culture with the chitinolytic bacterium Aeromonas hydrophila: parasitic growth of Pseudomonas aeruginosa. Environ Microbiol. 2010;12:1787–802.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Noto MJ, Burns WJ, Beavers WN, Skaar EP. Mechanisms of pyocyanin toxicity and genetic determinants of resistance in Staphylococcus aureus. J Bacteriol. 2017;199:00221–17.

  • Venkataraman A, Rosenbaum MA, Perkins SD, Werner JJ, Angenent LT. Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems. Energy Environ Sci. 2011;4:4550.

    CAS 
    Article 

    Google Scholar 

  • Waite RD, Qureshi MR, Whiley RA. Modulation of behaviour and virulence of a high alginate expressing Pseudomonas aeruginosa strain from cystic fibrosis by oral commensal bacterium Streptococcus anginosus. PLOS ONE. 2017;12:e0173741.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Whooley MA, McLoughlin AJ. The regulation of pyocyanin production in Pseudomonas aeruginosa. Eur J Appl Microbiol Biotechnol. 1982;15:161–6.

    CAS 
    Article 

    Google Scholar 

  • Elbargisy RM. Optimization of nutritional and environmental conditions for pyocyanin production by urine isolates of Pseudomonas aeruginosa. Saudi J Biol Sci. 2021;28:993–1000.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gupta S, Laskar N, Kadouri DE. Evaluating the effect of oxygen concentrations on antibiotic sensitivity, growth, and biofilm formation of human pathogens. Microbiol Insights. 2016;9. https://doi.org/10.4137/MBI.S40767.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Investig. 2002;109:317–25.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Skurnik D, Roux D, Cattoir V, Danilchanka O, Lu X, Yoder-Himes DR, et al. Enhanced in vivo fitness of carbapenem-resistant oprD mutants of Pseudomonas aeruginosa revealed through high-throughput sequencing. Proc Natl Acad Sci USA. 2013;110:20747–52.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Higgins S, Heeb S, Rampioni G, Fletcher MP, Williams P, Cámara M. Differential regulation of the phenazine biosynthetic operons by quorum sensing in Pseudomonas aeruginosa PAO1-N. Front Cell Infect Microbiol. 2018;8:252.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Dragoš A, Martin M, Falcón García C, Kricks L, Pausch P, Heimerl T, et al. Collapse of genetic division of labour and evolution of autonomy in pellicle biofilms. Nat Microbiol. 2018;3:1451–60.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Cuthbertson L, Walker AW, Oliver AE, Rogers GB, Rivett DW, Hampton TH, et al. Lung function and microbiota diversity in cystic fibrosis. Microbiome. 2020;8:45.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, Bruce KD. Characterization of bacterial community diversity in cystic fibrosis lung infections by use of 16S ribosomal DNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol. 2004;42:5176–83.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Workentine ML, Sibley CD, Glezerson B, Purighalla S, Norgaard-Gron JC, Parkins MD, et al. Phenotypic heterogeneity of Pseudomonas aeruginosa populations in a cystic fibrosis patient. PLoS ONE. 2013;8:e60225.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Valdezate S. Persistence and variability of Stenotrophomonas maltophilia in cystic fibrosis patients, Madrid, 1991-8. Emerg Infect Dis. 2001;7:113–22.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Dalbøge CS, Hansen CR, Pressler T, Høiby N, Johansen HK. Chronic pulmonary infection with Stenotrophomonas maltophilia and lung function in patients with cystic fibrosis. J Cyst Fibros. 2011;10:318–25.

    PubMed 
    Article 

    Google Scholar 

  • Jeon YD, Jeong WY, Kim MH, Jung IY, Ahn MY, Ann HW, et al. Risk factors for mortality in patients with Stenotrophomonas maltophilia bacteremia. Medicine. 2016;95:e4375.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Sherrard LJ, Tunney MM, Elborn JS. Antimicrobial resistance in the respiratory microbiota of people with cystic fibrosis. Lancet Lond Engl. 2014;384:703–13.

    CAS 
    Article 

    Google Scholar 

  • Choi K-H, Schweizer HP. Mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc. 2006;1:153–61.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Jelsbak L, Johansen HK, Frost A-L, Thøgersen R, Thomsen LE, Ciofu O, et al. Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect Immun. 2007;75:2214–24.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Yeung ATY, Parayno A, Hancock REW. Mucin promotes rapid surface motility in Pseudomonas aeruginosa. mBio. 2012;3:300073–12.

  • Kirchner S, Fothergill JL, Wright EA, James CE, Mowat E, Winstanley C. Use of artificial sputum medium to test antibiotic efficacy against Pseudomonas aeruginosa in conditions more relevant to the cystic fibrosis lung. J Vis Exp. 2012;64:3857.

  • Hill DB, Long RF, Kissner WJ, Atieh E, Garbarine IC, Markovetz MR, et al. Pathological mucus and impaired mucus clearance in cystic fibrosis patients result from increased concentration, not altered pH. Eur Respir J. 2018;52:1801297.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Benoni G, Cuzzolin L, Bertrand C, Puchetti V, Velo G. Imipenem kinetics in serum, lung tissue and pericardial fluid in patients undergoing thoracotomy. J Antimicrob Chemother. 1987;20:725–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Radhakrishnan M, Jaganath A, Rao GSU, Kumari HBV. Nebulized imipenem to control nosocomial pneumonia caused by Pseudomonas aeruginosa. J Crit Care. 2008;23:148–50.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wenzler E, Fraidenburg DR, Scardina T, Danziger LH. Inhaled antibiotics for gram-negative respiratory infections. Clin Microbiol Rev. 2016;29:581–632.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters.Version 12.0, 2022. http://www.eucast.org.

  • Kang D, Revtovich AV, Chen Q, Shah KN, Cannon CL, Kirienko NV. Pyoverdine-dependent virulence of Pseudomonas aeruginosa isolates from cystic fibrosis patients. Front Microbiol. 2019;10:2048.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Martin LW, Reid DW, Sharples KJ, Lamont IL. Pseudomonas siderophores in the sputum of patients with cystic fibrosis. BioMetals. 2011;24:1059–67.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Caldwell CC, Chen Y, Goetzmann HS, Hao Y, Borchers MT, Hassett DJ, et al. Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. Am J Pathol. 2009;175:2473–88.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • O’Loughlin CT, Miller LC, Siryaporn A, Drescher K, Semmelhack MF, Bassler BL. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci USA. 2013;110:17981–6.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Sass G, Nazik H, Penner J, Shah H, Ansari SR, Clemons KV, et al. Studies of Pseudomonas aeruginosa mutants indicate pyoverdine as the central factor in inhibition of Aspergillus fumigatus biofilm. J Bacteriol. 2018;200:00345–17.

  • Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Deatherage DE, Barrick JE. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. In: Sun L, Shou W, editors. Engineering and Analyzing Multicellular Systems. New York, NY: Springer New York; 2014. p. 165–88.

  • Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24–6.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013;14:178–92.

    CAS 
    PubMed 
    Article 

    Google Scholar 


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