The evolution of short- and long-range weapons for bacterial competition

  • Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, 1859).

  • Emlen, D. Animal Weapons: The Evolution of Battle (Picador, 2015).

  • Granato, E. T., Meiller-Legrand, T. A. & Foster, K. R. The evolution and ecology of bacterial warfare. Curr. Biol. 29, R521–R537 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • García-Bayona, L. & Comstock, L. E. Bacterial antagonism in host-associated microbial communities. Science 361, eaat2456 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Clardy, J., Fischbach, M. & Currie, C. The natural history of antibiotics. Curr. Biol. 19, R437–R441 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dulmage, H. T. The production of neomycin by Streptomyces fradiae in synthetic media. Appl. Microbiol. 1, 103–106 (1953).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schatz, A., Bugle, E. & Waksman, S. A. Streptomycin, a substance exhibiting antibiotic activity against gram-positive and gram-negative bacteria. Proc. Soc. Exp. Biol. Med. 55, 66–69 (1944).

    Article 
    CAS 

    Google Scholar
     

  • Westhoff, S. et al. Spatial structure increases the benefits of antibiotic production in Streptomyces. Evolution 74, 179–187 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wright, E. S. & Vetsigian, K. H. Inhibitory interactions promote frequent bistability among competing bacteria. Nat. Commun. 7, 11274 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ge, P. et al. Action of a minimal contractile bactericidal nanomachine. Nature 580, 658–662 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hachani, A. et al. Type VI secretion system in Pseudomonas aeruginosa. J. Biol. Chem. 286, 12317–12327 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ruhe, Z. C. et al. Programmed secretion arrest and receptor-triggered toxin export during antibacterial contact-dependent growth inhibition. Cell 175, 921–933.e14 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arbour, V. M., Zanno, L. E. & Evans, D. C. Palaeopathological evidence for intraspecific combat in ankylosaurid dinosaurs. Biol. Lett. 18, 20220404 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Livermore, D. M. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin. Infect. Dis. 34, 634–640 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ghequire, M. G. K. & De Mot, R. Ribosomally encoded antibacterial proteins and peptides from Pseudomonas. FEMS Microbiol. Rev. 38, 523–568 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sana, T. G., Berni, B. & Bleves, S. The T6SSs of Pseudomonas aeruginosa strain PAO1 and their effectors: beyond bacterial-cell targeting. Front. Cell. Infect. Microbiol. 6, 61 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chatzidaki-Livanis, M., Geva-Zatorsky, N. & Comstock, L. E. Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc. Natl Acad. Sci. USA 113, 3627–3632 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chatzidaki-Livanis, M. et al. Gut symbiont Bacteroides fragilis secretes a eukaryotic-like ubiquitin protein that mediates intraspecies antagonism. mBio 8, e01902–e01917 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bainton, N. J. et al. N-(3-Oxohexanoyl)-ʟ-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem. J. 288, 997–1004 (1992).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Poole, S. J. et al. Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet. 7, e1002217 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Myers-Morales, T., Oates, A. E., Byrd, M. S. & Garcia, E. C. Burkholderia cepacia complex contact-dependent growth inhibition systems mediate interbacterial competition. J. Bacteriol. 201, e00012–e00019 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ghequire, M. G. K. & De Mot, R. Distinct colicin M-like bacteriocin-immunity pairs in Burkholderia. Sci. Rep. 5, 17368 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Choi, S. Y. et al. Chromobacterium violaceum delivers violacein, a hydrophobic antibiotic, to other microbes in membrane vesicles. Environ. Microbiol. 22, 705–713 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Alves, J. A., Leal, F. C., Previato-Mello, M. & da Silva Neto, J. F. A quorum sensing-regulated type VI secretion system containing multiple nonredundant VgrG proteins is required for interbacterial competition in Chromobacterium violaceum. Microbiol. Spectr. 10, e0157622 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Troselj, V., Treuner-Lange, A., Søgaard-Andersen, L. & Wall, D. Physiological heterogeneity triggers sibling conflict mediated by the type VI secretion system in an aggregative multicellular bacterium. mBio 9, e01645-17 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xiao, Y., Gerth, K., Müller, R. & Wall, D. Myxobacterium-produced antibiotic TA (myxovirescin) inhibits type II signal peptidase. Antimicrob. Agents Chemother. 56, 2014–2021 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Celik Ozgen, V., Kong, W., Blanchard, A. E., Liu, F. & Lu, T. Spatial interference scale as a determinant of microbial range expansion. Sci. Adv. 4, eaau0695 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Smith, W. P. J. et al. The evolution of tit-for-tat in bacteria via the type VI secretion system. Nat. Commun. 11, 5395 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Smith, W. P. J. et al. The evolution of the type VI secretion system as a disintegration weapon. PLoS Biol. 18, e3000720 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Frost, I. et al. Cooperation, competition and antibiotic resistance in bacterial colonies. ISME J. 12, 1582–1593 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rudge, T. J., Steiner, P. J., Phillips, A. & Haseloff, J. Computational modeling of synthetic microbial biofilms. ACS Synth. Biol. 1, 345–352 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Smith, W. P. J. et al. Cell morphology drives spatial patterning in microbial communities. Proc. Natl Acad. Sci. USA 114, E280–E286 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Brown, S. P., Fredrik Inglis, R. & Taddei, F. SYNTHESIS: evolutionary ecology of microbial wars: within-host competition and (incidental) virulence. Evol. Appl. 2, 32–39 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chao, L. & Levin, B. R. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl Acad. Sci. USA 78, 6324–6328 (1981).

  • Teschler, J. K. et al. VxrB influences antagonism within biofilms by controlling competition through extracellular matrix production and type 6 secretion. mBio 13, e01885-22 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brown, S. P., Le Chat, L., De Paepe, M. & Taddei, F. Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Curr. Biol. 16, 2048–2052 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Durrett, R. & Levin, S. Allelopathy in spatially distributed populations. J. Theor. Biol. 185, 165–171 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Giometto, A., Nelson, D. R. & Murray, A. W. Antagonism between killer yeast strains as an experimental model for biological nucleation dynamics. eLife 10, e62932 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gordon, D. M. & Riley, M. A. A theoretical and empirical investigation of the invasion dynamics of colicinogeny. Microbiology 145, 655–661 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Levin, B. R. Frequency-dependent selection in bacterial populations. Phil. Trans. R. Soc. Lond. B 319, 459–472 (1988).

    Article 
    CAS 

    Google Scholar
     

  • Dorosky, R. J., Yu, J. M., Pierson, L. S. & Pierson, E. A. Pseudomonas chlororaphis produces two distinct R-tailocins that contribute to bacterial competition in biofilms and on roots. Appl. Environ. Microbiol. 83, e00706–e00717 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Oluyombo, O., Penfold, C. N. & Diggle, S. P. Competition in biofilms between cystic fibrosis isolates of Pseudomonas aeruginosa is shaped by R-pyocins. mBio 10, e01828-18 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Basler, M., Ho, B. T. & Mekalanos, J. J. Tit-for-tat: type VI secretion system counterattack during bacterial cell–cell interactions. Cell 152, 884–894 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wilton, M. et al. Chelation of membrane-bound cations by extracellular DNA activates the type VI secretion system in Pseudomonas aeruginosa. Infect. Immun. 84, 2355–2361 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mercy, C., Ize, B., Salcedo, S. P., de Bentzmann, S. & Bigot, S. Functional characterization of Pseudomonas contact dependent growth inhibition (CDI) systems. PLoS ONE 11, e0147435 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nakayama, K. et al. The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol. Microbiol. 38, 213–231 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Niehus, R., Oliveira, N. M., Li, A., Fletcher, A. G. & Foster, K. R. The evolution of strategy in bacterial warfare via the regulation of bacteriocins and antibiotics. eLife 10, e69756 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Köhler, T., Donner, V. & van Delden, C. Lipopolysaccharide as shield and receptor for R-pyocin-mediated killing in Pseudomonas aeruginosa. J. Bacteriol. 192, 1921–1928 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Borenstein, D. B., Ringel, P., Basler, M. & Wingreen, N. S. Established microbial colonies can survive type VI secretion assault. PLoS Comput. Biol. 11, e1004520 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Booth, S. C. & Rice, S. A. Influence of interspecies interactions on the spatial organization of dual species bacterial communities. Biofilm 2, 100035 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Branda, S. S., Vik, Å., Friedman, L. & Kolter, R. Biofilms: the matrix revisited. Trends Microbiol. 13, 20–26 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Flemming, H.-C. & Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 17, 247–260 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hallatschek, O., Hersen, P., Ramanathan, S. & Nelson, D. R. Genetic drift at expanding frontiers promotes gene segregation. Proc. Natl Acad. Sci. USA 104, 19926–19930 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hallatschek, O. & Nelson, D. R. Life at the front of an expanding population. Evolution 64, 193–206 (2010).

    Article 
    PubMed 

    Google Scholar
     

  • Mei, M., Thomas, J. & Diggle, S. P. Heterogenous susceptibility to R-pyocins in populations of Pseudomonas aeruginosa sourced from cystic fibrosis lungs. mBio 12, e00458-21 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Melvin, J. A. et al. Pseudomonas aeruginosa contact-dependent growth inhibition plays dual role in host–pathogen interactions. mSphere 2, e00336-17 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bottery, M. J., Passaris, I., Dytham, C., Wood, A. J. & van der Woude, M. W. Spatial organization of expanding bacterial colonies is affected by contact-dependent growth inhibition. Curr. Biol. 29, 3622–3634.e5 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sana, T. G. et al. Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc. Natl Acad. Sci. USA 113, E5044–E5051 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao, W., Caro, F., Robins, W. & Mekalanos, J. J. Antagonism toward the intestinal microbiota and its effect on Vibrio cholerae virulence. Science 359, 210–213 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hecht, A. L. Strain competition restricts colonization of an enteric pathogen and prevents colitis. EMBO Rep. 17, 1281–1291 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • LaCourse, K. D. et al. Conditional toxicity and synergy drive diversity among antibacterial effectors. Nat. Microbiol. 3, 440–446 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nadell, C. D., Drescher, K. & Foster, K. R. Spatial structure, cooperation and competition in biofilms. Nat. Rev. Microbiol. 14, 589–600 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rudge, T. J., Federici, F., Steiner, P. J., Kan, A. & Haseloff, J. Cell polarity-driven instability generates self-organized, fractal patterning of cell layers. ACS Synth. Biol. 2, 705–714 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ringel, P. D., Hu, D. & Basler, M. The role of type VI secretion system effectors in target cell lysis and subsequent horizontal gene transfer. Cell Rep. 21, 3927–3940 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sánchez-Romero, M. A. & Casadesús, J. Contribution of phenotypic heterogeneity to adaptive antibiotic resistance. Proc. Natl Acad. Sci. USA 111, 355–360 (2014).

    Article 
    PubMed 

    Google Scholar
     

  • Dötsch, A. et al. The Pseudomonas aeruginosa transcriptional landscape is shaped by environmental heterogeneity and genetic variation. mBio 6, e00749-15 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rojas, L. J. et al. Genomic heterogeneity underlies multidrug resistance in Pseudomonas aeruginosa: a population-level analysis beyond susceptibility testing. PLoS ONE 17, e0265129 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bucci, V., Nadell, C. D. & Xavier, J. B. The evolution of bacteriocin production in bacterial biofilms. Am. Nat. 178, E162–E173 (2011).

    Article 
    PubMed 

    Google Scholar
     

  • Westhoff, S., Kloosterman, A. M., van Hoesel, S. F. A., van Wezel, G. P. & Rozen, D. E. Competition sensing changes antibiotic production in Streptomyces. mBio 12, e02729–20 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cornforth, D. M. & Foster, K. R. Competition sensing: the social side of bacterial stress responses. Nat. Rev. Microbiol. 11, 285–293 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • LeRoux, M., Peterson, S. B. & Mougous, J. D. Bacterial danger sensing. J. Mol. Biol. 427, 3744–3753 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Konisky, J. & Richards, F. M. Characterization of colicin Ia and colicin Ib: purification and some physical properties. J. Biol. Chem. 245, 2972–2978 (1970).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Choi, K.-H. & Schweizer, H. P. An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol. 5, 30 (2005).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rietsch, A., Vallet-Gely, I., Dove, S. L. & Mekalanos, J. J. ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 102, 8006–8011 (2005).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Harms, A. et al. A bacterial toxin–antitoxin module is the origin of inter-bacterial and inter-kingdom effectors of Bartonella. PLoS Genet. 13, e1007077 (2017).

    Article 
    PubMed 
    PubMed Central 

    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).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Silva-Rocha, R. et al. The Standard European Vector Architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes. Nucleic Acids Res. 41, D666–D675 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nadell, C. D., Xavier, J. B. & Foster, K. R. The sociobiology of biofilms. FEMS Microbiol. Rev. 33, 206–224 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Greig, D. & Travisano, M. Density-dependent effects on allelopathic interactions in yeast. Evolution 62, 521–527 (2008).

    Article 
    PubMed 

    Google Scholar
     

  • Rendueles, O., Amherd, M. & Velicer, G. J. Positively frequency-dependent interference competition maintains diversity and pervades a natural population of cooperative microbes. Curr. Biol. 25, 1673–1681 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krishna Kumar, R. et al. Droplet printing reveals the importance of micron-scale structure for bacterial ecology. Nat. Commun. 12, 857 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McNally, L. et al. Killing by type VI secretion drives genetic phase separation and correlates with increased cooperation. Nat. Commun. 8, 14371 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • van Gestel, J., Weissing, F. J., Kuipers, O. P. & Kovács, Á. T. Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms. ISME J. 8, 2069–2079 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wickham, H. et al. Welcome to the tidyverse. J. Open Source Softw. 4, 1686 (2019).

    Article 

    Google Scholar
     

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

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Reference

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