A single mutation in rapP induces cheating to prevent cheating in Bacillus subtilis by minimizing public good production

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Cooperation is beneficial to group behaviors like multicellularity, but is vulnerable to exploitation by cheaters. Here we analyze mechanisms that protect against exploitation of extracellular surfactin in swarms of Bacillus subtilis. Unexpectedly, the reference strain NCIB 3610 displays inherent resistance to surfactin-non-producing cheaters, while a different wild isolate is susceptible. We trace this interstrain difference down to a single amino acid change in the plasmid-borne regulator RapP, which is necessary and sufficient for cheater mitigation. This allele, prevalent in many Bacillus species, optimizes transcription of the surfactin operon to the minimum needed for full cooperation. When combined with a strain lacking rapP, NCIB 3610 acts as a cheater itself—except it does not harm the population at high proportions since it still produces enough surfactin. This strategy of minimal production is thus a doubly advantageous mechanism to limit exploitation of public goods, and is readily evolved from existing regulatory networks.