Background Evolutionary arms race plays a major role in shaping biological diversity. In microbial systems, competition often involves chemical warfare and the production of bacteriocins, narrow-spectrum toxins aimed at killing closely related strains by forming pores in their target’s membrane or by degrading the target’s RNA or DNA. Although many empirical and theoretical studies describe competitive exclusion of bacteriocin-sensitive strains by producers of bacteriocins, the dynamics among producers are largely unknown. Methodology/Principal findings We used a reporter-gene assay to show that the bacterial response to bacteriocins’ treatment mirrors the inflicted damage Potent bacteriocins are lethal to competing strains, but at sublethal doses can serve as strong inducing agents, enhancing their antagonists’ bacteriocin production. In contrast, weaker bacteriocins are less toxic to their competitors and trigger mild bacteriocin expression. We used empirical and numerical models to explore the role of cross-induction in the arms race between bacteriocin-producing strains. We found that in well-mixed, unstructured environments where interactions are global, producers of weak bacteriocins are selectively advantageous and outcompete producers of potent bacteriocins. However, in spatially structured environments, where interactions are local, each producer occupies its own territory, and competition takes place only in “no man’s lands” between territories, resulting in much slower dynamics. Conclusion/Significance The models we present imply that producers of potent bacteriocins that trigger a strong response in neighboring bacteriocinogenic strains are doomed, while producers of weak bacteriocins that trigger a mild response in bacteriocinogenic strains flourish. This counter-intuitive outcome might explain the preponderance of weak bacteriocin producers in nature. However, the described scenario is prolonged in spatially structured environments thus promoting coexistence, allowing migration and evolution, and maintaining bacterial diversity.
References
[1]
Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Micro 8: 15–25.
[2]
de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29: 795–811.
[3]
Riley MA, Chavan MA (2007) Bacteriocins: Ecology and Evolution. Bacteriocins: Ecology and Evolution.
[4]
Kerr B, Riley MA, Feldman MW, Bohannan BJ (2002) Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418: 171–174.
[5]
Gordon DM, Riley MA (1999) A theoretical and empirical investigation of the invasion dynamics of colicinogeny. Microbiology 145: 655–661.
[6]
Lenski RE, Riley MA (2002) Chemical warfare from an ecological perspective. Proc Natl Acad Sci U S A 99: 556–558.
Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56: 117–137.
[9]
Inglis RF, Gardner A, Cornelis P, Buckling A (2009) Spite and virulence in the bacterium Pseudomonas aeruginosa. Proc Natl Acad Sci USA 106: 5703–5707.
[10]
Mulec J, Podlesek Z, Mrak P, Kopitar A, Ihan A, et al. (2003) A cka-gfp transcriptional fusion reveals that the colicin K activity gene is induced in only 3 percent of the population. J Bacteriol 185: 654–659.
Chao L, Levin BR (1981) Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci USA 78: 6324–6328.
[13]
Frank SA (1994) Spatial polymorphism of bacteriocins and other allelopathic traits Evol Ecol. 8: 369–386.
[14]
Kirkup BC, Riley MA (2004) Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature 428: 412–414.
[15]
Durrett R, Levin S (1997) Allelopathy in spatially distributed populations. J Theor Biol 185: 165–171.
[16]
Barnes B, Sidhu H, Gordon DM (2007) Host gastro-intestinal dynamics and the frequency of colicin production by Escherichia coli. Microbiology 153: 2823–2827.
[17]
Gordon DM, O’Brien CL (2006) Bacteriocin diversity and the frequency of multiple bacteriocin production in Escherichia coli. Microbiology 152: 3239–3244.
[18]
Riley MA, Gordon DM (1992) A survey of Col plasmids in natural isolates of Escherichia coli and an investigation into the stability of Col-plasmid lineages. J Gen Microbiol 138 1345–1352.
[19]
Riley MA, Gordon DM (1999) The ecological role of bacteriocins in bacterial competition. Trends Microbiol 7: 129–133.
[20]
Majeed H, Gillor O, Kerr B, Riley MA (2011) Competitive interactions in Escherichia coli populations: the role of bacteriocins. ISME J 5: 71–81.
[21]
Pugsley AP (1985) Escherichia coli K12 strains for use in the identification and characterization of colicins. J Gen Microbiol 131: 369–376.
[22]
Gillor O, Vriezen JAC, Riley MA (2008) The role of SOS boxes in enteric bacteriocin regulation. Microbiology 154: 1783–1792.
[23]
Van Dyk TK, Rosson RA (1998) Photorhabdus luminescens luxCDABE promoter probe vectors. Methods in Molecular Biology; Bioluminescence methods and protocols: 85–95.
[24]
Van Dyk TK, DeRose EJ, Gonye GE (2001) LuxArray, a high-density, genomewide transcription analysis of Escherichia coli using bioluminescent reporter strains. J Bacteriol 183: 5496–5505.
[25]
Zaslaver A, Bren A, Ronen M, Itzkovitz S, Kikoin I, et al. (2006) A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Methods 3: 623–628.
[26]
Suit JL, Fan MLJ, Sabik JF, Labarre R, Luria SE (1983) Alternative forms of lethality in mitomycin C-induced bacteria carrying ColE1 plasmids. Proc Natl Acad Sci USA 80: 579–583.
[27]
Cormack BP, Valdivia RH, Falkow S (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33–38.
[28]
Graille M, Mora L, Buckingham RH, van Tilbeurgh H, de Zamaroczy M (2004) Structural inhibition of the colicin D tRNase by the tRNA-mimicking immunity protein. EMBO J 23: 1474–1482.
[29]
Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797–810.
[30]
Kleanthous C (2011) Swimming against the tide: progress and challenges in our understanding of colicin translocation. Nat Rev Microbiol 8: 843–848.
[31]
Walker D, Rolfe M, Thompson A, Moore GR, James R, et al. (2004) Transcriptional profiling of colicin-induced cell death of Escherichia coli MG1655 identifies potential mechanisms by which bacteriocins promote bacterial diversity. J Bacteriol 186: 866–869.
[32]
Siepielski AM, McPeek MA (2010) On the evidence for species coexistence: a critique of the coexistence program. Ecology 91: 3153–3164.
[33]
Vellend M, Geber MA (2005) Connections between species diversity and genetic diversity. Ecol Lett 8: 767–781.
[34]
West SA, Diggle SP, Buckling A, Gardner A, Griffins AS (2007) The social lives of microbes. Annu Rev Ecol, Evol Syst 38: 53–77.
[35]
Gardner A, West SA, Buckling A (2004) Bacteriocins, spite and virulence. Proceedings of the Royal Society of London Series B: Biological Sciences 271: 1529–1535.
[36]
West SA, Gardner A (2010) Altruism, Spite, and Greenbeards. Science 327: 1341–1344.
