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Abstract
Biofilms are multispecies communities, in which bacteria constantly compete with one another for resources and niches. Bacteria produce many antibiotics and toxins for competition. However, since biofilm cells exhibit increased tolerance to antimicrobials, their roles in biofilms remain controversial. Here, we showed that Bacillus subtilis produces multiple diverse polymorphic toxins, called LXG toxins, that contain N-terminal LXG delivery domains and diverse C-terminal toxin domains. Each B. subtilis strain possesses a distinct set of LXG toxin–antitoxin genes, the number and variation of which is sufficient to distinguish each strain. The B. subtilis strain NCIB3610 possesses six LXG toxin–antitoxin operons on its chromosome, and five of the toxins functioned as DNase. In competition assays, deletion mutants of any of the six LXG toxin–antitoxin operons were outcompeted by the wild-type strain. This phenotype was suppressed when the antitoxins were ectopically expressed in the deletion mutants. The fitness defect of the mutants was only observed in solid media that supported biofilm formation. Biofilm matrix polymers, exopolysaccharides and TasA protein polymers were required for LXG toxin function. These results indicate that LXG toxin-antitoxin systems specifically mediate intercellular competition between B. subtilis strains in biofilms. Mutual antagonism between some LXG toxin producers drove the spatial segregation of two strains in a biofilm, indicating that LXG toxins not only mediate competition in biofilms, but may also help to avoid warfare between strains in biofilms. LXG toxins from strain NCIB3610 were effective against some natural isolates, and thus LXG toxin–antitoxin systems have ecological impact. B. subtilis possesses another polymorphic toxin, WapA. WapA had toxic effects under planktonic growth conditions but not under biofilm conditions because exopolysaccharides and TasA protein polymers inhibited WapA function. These results indicate that B. subtilis uses two types of polymorphic toxins for competition, depending on the growth mode.
Highlights
Like many life-forms, bacteria are social organisms that must constantly compete or cooperate with each other
Biofilms are surface-associated multispecies communities, in which bacteria are protected by self-produced extracellular polymeric substances
We found that the soil bacterium B. subtilis produces polymorphic toxins, termed LXG toxins
Summary
Like many life-forms, bacteria are social organisms that must constantly compete or cooperate with each other These interactions play critical roles in surface-associated bacterial communities, termed biofilms. Multispecies biofilms are believed to develop through a series of intra- and interspecies interactions In these interactions, bacteria distance from or outcompete unfavorable competitors and promote beneficial neighbors to increase their fitness. Unfavorable competitors are often the same or closely related species because they share genetic traits and preferred niches [1,5]. Another kind of unfavorable competitors are “freeloading cheaters”, which consume extracellular products such as polymeric substances, enzymes, metabolites, and signaling molecules without contributing themselves [5]. Competition and kin discrimination mechanisms in biofilms remain to be elucidated
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