Abstract
Production of public goods in biological systems is often a collaborative effort that may be detrimental to the producers. It is therefore sustainable only if a small fraction of the population shoulders the cost while the majority reap the benefits. We modelled this scenario using Escherichia coli populations producing colicins, an antibiotic that kills producer cells’ close relatives. Colicin expression is a costly trait, and it has been proposed that only a small fraction of the population actively expresses the antibiotic. Colicinogenic populations were followed at the single-cell level using time-lapse microscopy, and showed two distinct, albeit dynamic, subpopulations: the majority silenced colicin expression, while a small fraction of elongated, slow-growing cells formed colicin-expressing hotspots, placing a significant burden on expressers. Moreover, monitoring lineages of individual colicinogenic cells showed stochastic switching between expressers and non-expressers. Hence, colicin expressers may be engaged in risk-reducing strategies—or bet-hedging—as they balance the cost of colicin production with the need to repel competitors. To test the bet-hedging strategy in colicin-mediated interactions, competitions between colicin-sensitive and producer cells were simulated using a numerical model, demonstrating a finely balanced expression range that is essential to sustaining the colicinogenic population.
Highlights
An alternative strategy for bacteriocinogenic populations is proposed: they hedge their bets by phenotypically alternating between expressers and non-expressers of bacteriocins
Isogenic strains lacking the colicin operon but hosting a reporter vector regulated by colicin E2 promoter were used as controls—these were chosen for their classical structure[16]
The prevailing model of colicin production asserts that colicinogenic populations are heterogeneous, as a small subset expresses large amounts of colicin, which increase during induction[17,19,20,22,23]
Summary
An alternative strategy for bacteriocinogenic populations is proposed: they hedge their bets by phenotypically alternating between expressers and non-expressers of bacteriocins. The high cost imposed by colicin production suggests that extensive measures are required to avoid it by tightly controlling expression[15,16] Another measure suggested to compensate for the cost associated with production colicins is the ‘division of labor’ as only a very small fraction of the population express colicin, whereas most of the cells silence expression, suggesting phenotypic heterogeneity[17]. The colicin expressers were significantly different from their non-expressing clone mates, probably because their DNA was damaged, inducing the SOS response system[22,23]. We predicted that these expressers persist until enough lysis proteins accumulate to lyse the producer cell, releasing colicins into the media. We hypothesised that different colicinogenic strains would diverge in their expression patterns in accordance with the differences in their regulatory elements[16,26,27,28] and modes of action[6]
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