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Coordination of siderophore gene expression among clonal cells of the bacterium Pseudomonas aeruginosa

  • West, S. A., Diggle, S. P., Buckling, A., Gardner, A. & Griffin, A. S. The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38, 53–77 (2007).

    Article 

    Google Scholar 

  • Diggle, S. P., Griffin, A. S., Campell, G. S. & West, S. A. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411–414 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ebrahimi, A., Schwartzman, J. & Cordero, O. X. Cooperation and spatial self-organization determine rate and efficiency of particulate organic matter degradation in marine bacteria. Proc. Natl Acad. Sci. USA 116, 23309–23316 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Yan, J., Monaco, H. & Xavier, J. B. The ultimate guide to bacterial swarming: An experimental model to study the evolution of cooperative behavior. Annu. Rev. Microbiol. 73, 293–312 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Kramer, J., Özkaya, Ö. & Kümmerli, R. Bacterial siderophores in community and host interactions. Nat. Rev. Microbiol. 18, 152–163 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Griffin, A., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Sandoz, K. M., Mitzimberg, S. M. & Schuster, M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl Acad. Sci. USA 104, 15876–15881 (2007).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Xavier, J. B., Kim, W. & Foster, K. R. A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol. Microbiol. 79, 166–179 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Drescher, K., Nadell, C. D., Stone, H. A., Wingreen, N. S. & Bassler, B. L. Solutions to the public goods dilemma in bacterial biofilms. Curr. Biol. 24, 50–55 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Nadal Jimenez, P. et al. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 76, 46–65 (2012).

    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Schuster, M., Sexton, D. J., Diggle, S. P. & Greenberg, E. P. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu. Rev. Microbiol. 67, 43–63 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Papenfort, K. & Bassler, B. L. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14, 576–588 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Darch, S. E., West, S. A., Winzer, K. & Diggle, S. P. Density-dependent fitness benefits in quorum-sensing bacterial populations. Proc. Natl Acad. Sci. USA 109, 8259–8263 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ross-Gillespie, A. & Kümmerli, R. Collective decision-making in microbes. Front. Microbiol. 5, 54 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Whiteley, M., Diggle, S. P. & Greenberg, E. P. Progress in and promise of bacterial quorum sensing research. Nature 551, 313–320 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Avery, A. Microbial cell individuality and the underlying sources of heterogeneity. Nat. Rev. Microbiol. 4, 577–587 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Eldar, A. & Elowitz, M. B. Functional roles for noise in genetic circuits. Nature 467, 167–173 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ackermann, M. A functional perspective on phenotypic heterogeneity in microorganisms. Nat. Rev. Microbiol. 13, 497–508 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Visca, P., Imperi, F. & Lamont, I. L. Pyoverdine siderophores: From biogenesis to biosignificance. Trends Microbiol. 15, 22–30 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Youard, Z. A., Wenner, N. & Reimmann, C. Iron acquisition with the natural siderophore enantiomers pyochelin and enantio-pyochelin in Pseudomonas species. Biometals 24, 513–522 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Schalk, I. J. & Cunrath, O. An overview of the biological metal uptake pathways in Pseudomonas aeruginosa. Environ. Microbiol. 18, 3227–3246 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Schalk, I. J., Rigouin, C. & Godet, J. An overview of siderophore biosynthesis among fluorescent Pseudomonads and new insights into their complex cellular organization. Environ. Microbiol. 22, 1447–1466 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Ochsner, U. A. & Vasil, M. L. Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: Cycle selection of iron-regulated genes. Proc. Natl Acad. Sci. USA 93, 4409–4414 (1996).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Leoni, L., Ciervo, A., Orsi, N. & Visca, P. Iron-regulated transcription of the pvdA gene in Pseudomonas aeruginosa: effect of Fur and PvdS on promoter activity. J. Bacteriol. 178, 2299–2313 (1996).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Escolar, L., Pérez-Martín, J. & de Lorenzo, V. Opening the iron box: Transcriptional metalloregulation by the fur protein. J. Bacteriol. 181, 6223–6229 (1999).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Dumas, Z., Ross-Gillespie, A. & Kümmerli, R. Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc. R. Soc. B 280, 20131055 (2013).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Lamont, I. L., Beare, P., Ochsner, U., Vasil, A. I. & Vasil, M. L. Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 99, 7072–7077 (2002).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Edgar, R. J. et al. Interactions between an anti-sigma protein and two sigma factors that regulate the pyoverdine signaling pathway in Pseudomonas aeruginosa. BMC Microbiol. 14, 287 (2014).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Heinrichs, D. E. & Poole, K. Cloning and sequence analysis of a gene (pchR) encoding an AraC family activator of pyochelin and ferripyochelin receptor synthesis in Pseudomonas aeruginosa. J. Bacteriol. 175, 5882–5889 (1993).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Michel, L., Gonzalez, N., Jagdeep, S., Nguyen-Ngoc, T. & Reimmann, C. PchR-box recognition by the AraC-type regulator PchR of Pseudomonas aeruginosa requires the siderophore pyochelin as an effector. Microbiology 58, 495–509 (2005).

    CAS 

    Google Scholar 

  • Michel, L., Bachelard, A. & Reimmann, C. Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Pseudomonas aeruginosa. Microbiology 153, 1508–1518 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Cornelis, P. & Dingemans, J. Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front. Cell. Infect. Microbiol. 3, 75 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Brandel, J. et al. Pyochelin, a siderophore of Pseudomonas aeruginosa: Physicochemical characterization of the iron(III), copper(II) and zinc(II) complexes. Dalton Trans. 41, 2820–2834 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Perraud, Q. et al. Phenotypic adaptation of Pseudomonas aeruginosa in the presence of siderophore-antibiotic conjugates during epithelial cell infection. Microorganisms 8, 1820 (2020).

    CAS 
    PubMed Central 
    Article 

    Google Scholar 

  • Mossialos, D. et al. Quinolobactin, a new siderophore of Pseudomonas fluorescens ATCC 17400, the production of which Is repressed by the cognate pyoverdine. Appl. Environ. Microbiol. 66, 487–492 (2000).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Tyrrell, J. et al. Investigation of the multifaceted iron acquisition strategies of Burkholderia cenocepacia. BioMetals 28, 367–380 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wei, Q. et al. Global regulation of gene expression by OxyR in an important human opportunistic pathogen. Nucleic Acids Res. 40, 4320–4333 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Frangipani, E. et al. The Gac/Rsm and cyclic-di-GMP signalling networks coordinately regulate iron uptake in Pseudomonas aeruginosa. Environ. Microbiol. 16, 676–688 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Schulz, S. et al. Elucidation of sigma factor-associated networks in Pseudomonas aeruginosa reveals a modular architecture with limited and function-specific crosstalk. PLoS Pathog. 11, e1004744 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Cunrath, O. et al. The pathogen Pseudomonas aeruginosa optimizes the production of the siderophore pyochelin upon environmental challenges. Metallomics 12, 2108–2120 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wang, T. et al. An atlas of the binding specificities of transcription factors in Pseudomonas aeruginosa directs prediction of novel regulators in virulence. eLife 10, e61885 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Tiburzi, F., Imperi, F. & Visca, P. Intracellular levels and activity of PvdS, the major iron starvation sigma factor of Pseudomonas aeruginosa. Mol. Microbiol. 67, 213–227 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kümmerli, R., Jiricny, N., Clarke, L. S., West, S. A. & Griffin, A. S. Phenotypic plasticity of a cooperative behaviour in bacteria. J. Evol. Biol. 22, 589–598 (2009).

    PubMed 
    Article 

    Google Scholar 

  • Harrison, F. Dynamic social behaviour in a bacterium: Pseudomonas aeruginosa partially compensates for siderophore loss to cheats. J. Evol. Biol. 26, 1370–1378 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Schiessl, K. T. et al. Individual- versus group-optimality in the production of secreted bacterial compounds. Evolution 73, 675–688 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Cunrath, O. et al. A cell biological view of the siderophore pyochelin iron uptake pathway in Pseudomonas aeruginosa. Environ. Microbiol. 17, 171–185 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Leinweber, A., Weigert, M. & Kümmerli, R. The bacterium Pseudomonas aeruginosa senses and gradually responds to interspecific competition for iron. Evolution 72, 1515–1528 (2018).

    CAS 
    PubMed Central 
    Article 

    Google Scholar 

  • Julou, T. et al. Cell-cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies. Proc. Natl Acad. Sci. USA 110, 12577–12582 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Weigert, M. & Kümmerli, R. The physical boundaries of public goods cooperation between surface-attached bacterial cells. Proc. R. Soc. B 284, 20170631 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Jayaraman, P., Sakharkar, M. K., Lim, C. S., Hock Tang, T. & Sakharkar, K. R. Activity and interactions of antibiotic and phytochemical combinations against Pseudomonas aeruginosa in vitro. Int. J. Biol. Sci. 6, 556–568 (2010).

  • Kapoor, G., Saigal, S. & Elongavan, A. Action and resistance mechanisms of antibiotics: A guide for clinicians. J. Anaesthesiol. Clin. Pharmacol. 33, 300–305 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Wrobel, A., Arciszewska, K., Maliszewski, D. & Drozdowska, D. Trimethoprim and other nonclassical antifolates an excellent template for searching modifications of dihydrofolate reductase enzyme inhibitors. J. Antibiot. 73, 5–27 (2020).

    CAS 
    Article 

    Google Scholar 

  • van der Veen, D. R. et al. Flexible clock systems: Adjusting the temporal programme. Phil. Trans. R. Soc. B 372, 20160254 (2017).

  • Helm, B. et al. Two sides of a coin: ecological and chronobiological perspectives of timing in the wild. Phil. Trans. R. Soc. B 372, 0246 (2017).

  • Rivera, M. Bacterioferritin: structure, dynamics, and protein–protein interactions at play in iron storage and mobilization. Acc. Chem. Res. 50, 331–340 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Soldano, A., Yao, H., Chandler, J. R. & Rivera, M. Inhibiting iron mobilization from bacterioferritin in Pseudomonas aeruginosa impairs biofilm formation irrespective of environmental iron availability. ACS Infectious Dis. 6, 447–458 (2020).

  • Andrews, S. C., Robinson, A. K. & Rodriguez-Quinones, F. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27, 215–237 (2003).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Alqarni, B., Colley, B., Klebensberger, J., McDougald, D. & Rice, S. A. Expression stability of 13 housekeeping genes during carbon starvation of Pseudomonas aeruginosa. J. Microbiol. Methods 127, 182–187 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Veening, J.-W., Smits, W. K. & Kuipers, O. P. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62, 193–210 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ratcliff, W. C. & Denison, R. F. Individual-level bet hedging in the bacterium Sinorhizobium meliloti. Curr. Biol. 20, 1740–1744 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Schreiber, F. et al. Phenotypic heterogeneity driven by nutrient limitation promotes growth in fluctuating environments. Nat. Microbiol. 1, 16055 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Conradt, L. & Roper, T. J. Consensus decision making in animals. Trends Ecol. Evol. 20, 449–456 (2005).

    PubMed 
    Article 

    Google Scholar 

  • Sumpter, D. J. T. The principles of collective animal behaviour. Philos. Trans. R. Soc. B 361, 5–22 (2006).

    CAS 
    Article 

    Google Scholar 

  • Couzin, I. D. Collective cognition in animal groups. Trends Cogn. Sci. 13, 36–43 (2009).

    PubMed 
    Article 

    Google Scholar 

  • Bose, T., Reina, A. & Marshall, J. A. R. Collective decision-making. Curr. Opin. Behav. Sci. 16, 30–34 (2017).

    Article 

    Google Scholar 

  • Dussutour, A., Ma, Q. & Sumpter, D. Phenotypic variability predicts decision accuracy in unicellular organisms. Proc. R. Soc. B 286, 20182825 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ross-Gillespie, A., Dumas, Z. & Kümmerli, R. Evolutionary dynamics of interlinked public goods traits: an experimental study of siderophore production in Pseudomonas aeruginosa. J. Evol. Biol. 28, 29–39 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Choi, K.-H. & Schweizer, H. P. mini-Tn7 insertion in bacteria with single attTn7 sites: Example Pseudomonas aeruginosa. Nat. Protoc. 1, 153–161 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Rezzoagli, C., Granato, E. T. & Kümmerli, R. In-vivo microscopy reveals the impact of Pseudomonas aeruginosa social interactions on host colonization. ISME J. 13, 2403–2414 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Minoia, M. et al. Stochasticity and bistability in horizontal transfer control of a genomic island in Pseudomonas. Proc. Natl Acad. Sci. USA 105, 20792–20797 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Mellini, M. et al. Generation of genetic tools for gauging multiple-gene expression at the single-cell level. Appl. Environ. Microbiol. 87, e02956–02920 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Li, S., Crooks, P. A., Wei, X. & de Leon, J. Toxicity of dipyridyl compounds and related compounds. Crit. Rev. Toxicol. 34, 447–460 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Liu, Y., Yang, L. & Molin, S. Synergistic activities of an efflux pump inhibitor and iron chelators against Pseudomonas aeruginosa growth and biofilm formation. Antimicrob. Agents Chemother. 54, 3960–3963 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Henriquez, T., Stein, N. V. & Jung, H. Resistance to bipyridyls mediated by the TtgABC efflux system in Pseudomonas putida KT2440. Front. Microbiol. 11, 1974 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Meyer, J.-M., Neely, A., Stintzi, A., Georges, C. & Holder, I. A. Pyoverdin is essential for viruence of Pseudomonas aeruginosa. Infect. Immun. 64, 518–523 (1996).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • de Jong, I. G., Beilharz, K., Kuipers, O. P. & Veening, J. W. Live cell imaging of Bacillus subtilis and Streptococcus pneumoniae using automated time-lapse microscopy. J. Vis. Exp. 53, e3145 (2011).

    Google Scholar 

  • Berg, S. et al. ilastik: Interactive machine learning for (bio)image analysis. Nat. Methods 16, 1226–1232 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

  • Mridha, S. and Kuemmerli, R. Mridha_Kummerli_2022_CommsBiol_raw_data_figshare.xlsx. figshare. Dataset. https://doi.org/10.6084/m9.figshare.19681962.v1 (2022)


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