Social Interactions and Distribution of Bacillus subtilis Pherotypes at Microscale

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Bacteria coordinate their behavior using quorum sensing (QS), whereby cells secrete diffusible signals that generate phenotypic responses associated with group living. The canonical model of QS is one of extracellular signaling, where signal molecules bind to cognate receptors and cause a coordinated response across many cells. Here we study the link between QS input (signaling) and QS output (response) in the ComQXPA QS system of Bacillus subtilis by characterizing the phenotype and fitness of comQ null mutants. These lack the enzyme to produce the ComX signal and do not activate the ComQXPA QS system in other cells. In addition to the activation effect of the signal, however, we find evidence of a second, repressive effect of signal production on the QS system. Unlike activation, which can affect other cells, repression acts privately: the de-repression of QS in comQ cells is intracellular and only affects mutant cells lacking ComQ. As a result, the QS signal mutants have an overly responsive QS system and overproduce the secondary metabolite surfactin in the presence of the signal. This surfactin overproduction is associated with a strong fitness cost, as resources are diverted away from primary metabolism. Therefore, by acting as a private QS repressor, ComQ may be protected against evolutionary competition from loss-of-function mutations. Additionally, we find that surfactin participates in a social selection mechanism that targets signal null mutants in coculture with signal producers. Our study shows that by pleiotropically combining intracellular and extracellular signaling, bacteria may generate evolutionarily stable QS systems.social interactions | social evolution B acteria secrete and share quorum-sensing (QS) signaling molecules that bind to specific receptors, and upon reaching critical concentration induce cell density-dependent adaptive responses within the population (1). In Gram-positive bacteria small peptide QS signals are typically produced from oligopeptide precursors that are modified by a signal-processing enzyme before they are secreted from the cell. It is assumed that these bacteria secrete QS signals during growth, and then in the stationary phase when the signal threshold concentration is reached, the signals activate specific histidine kinase receptors. These activate specific response regulators through phosphotransfer, which then initiate a QS response (2). The QS response often involves expression of adaptive extracellular factors (such as food-degrading enzymes, virulence factors, antibiotics, or biosurfactants) that are considered public goods (3, 4), as they can be shared within the population. Recently, however, it was shown that the QS of Gramnegative bacteria may also regulate adaptive metabolic pathways that produce molecules that remain private as they are not secreted by the responsive cells (5).The ComQXPA QS system of Bacillus subtilis is a typical QS system of Gram-positive bacteria that controls expression of nearly 200 genes, including both extracellular and private...

Section: Discussionmentioning

confidence: 58%

Private link between signal and response in Bacillus subtilis quorum sensing

Oslizlo

Štefanič

Dogša

et al. 2014

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“…Our collection of 39 B. subtilis strains was isolated from two closely located 1-cm 3 soil samples (21) where strains in close proximity may have had a history of interaction. The collection is therefore ideal to correlate swarming interactions with other properties of the strains such as genetic relatedness and ecotype affiliations.…”

Section: Swarms Affiliated With Different Ecotypes Recognize Each Othmentioning

confidence: 99%

Kin discrimination between sympatric Bacillus subtilis isolates

Štefanič

Kraigher

Lyons

et al. 2015

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125

204

Kin discrimination, broadly defined as differential treatment of conspecifics according to their relatedness, could help biological systems direct cooperative behavior toward their relatives. Here we investigated the ability of the soil bacterium Bacillus subtilis to discriminate kin from nonkin in the context of swarming, a cooperative multicellular behavior. We tested a collection of sympatric conspecifics from soil in pairwise combinations and found that despite their history of coexistence, the vast majority formed distinct boundaries when the swarms met. Some swarms did merge, and most interestingly, this behavior was only seen in the most highly related strain pairs. Overall the swarm interaction phenotype strongly correlated with phylogenetic relatedness, indicative of kin discrimination. Using a subset of strains, we examined cocolonization patterns on plant roots. Pairs of kin strains were able to cocolonize roots and formed a mixed-strain biofilm. In contrast, inoculating roots with pairs of nonkin strains resulted in biofilms consisting primarily of one strain, suggestive of an antagonistic interaction among nonkin strains. This study firmly establishes kin discrimination in a bacterial multicellular setting and suggests its potential effect on ecological interactions.swarming | biofilm | social evolution | kin recognition | antagonism

“…Pherotypes differ in their receptor-autoinducer specificity but not in the pathways regulated by the receptor. In addition, many pherotypes show patterns of intraspecific horizontal gene transfer (10,12) and coexist in the same environment (15,16).…”

mentioning

confidence: 99%

“…This system is encoded by a single locus that contains a three-gene operon. The ComX autoinducer production genes (comQ, comX) and the region of comP encoding for the extracellular part of the ComP receptor are highly variable and encode for multiple different pherotypes, which coexist in the soil and undergo rapid horizontal gene transfer (10,15,16,20). The interaction between different comQXP pherotypes also includes cases of asymmetric cross-activation or cross-inhibition, where a ComX autoinducer of one pherotype would activate the receptor of another pherotype, but not vice versa, or when the autoinducer inhibits the receptor of another pherotype (10,20).…”

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confidence: 99%

Facultative cheating supports the coexistence of diverse quorum-sensing alleles

Pollak

Omer-Bendori

Even-Tov

et al. 2016

Bacterial quorum sensing enables bacteria to cooperate in a densitydependent manner via the group-wide secretion and detection of specific autoinducer molecules. Many bacterial species show high intraspecific diversity of autoinducer-receptor alleles, called pherotypes. The autoinducer produced by one pherotype activates its coencoded receptor, but not the receptor of another pherotype. It is unclear what selection forces drive the maintenance of pherotype diversity. Here, we use the ComQXPA system of Bacillus subtilis as a model system, to show that pherotype diversity can be maintained by facultative cheating-a minority pherotype exploits the majority, but resumes cooperation when its frequency increases. We find that the maintenance of multiple pherotypes by facultative cheating can persist under kin-selection conditions that select against "obligate cheaters" quorum-sensing response null mutants. Our results therefore support a role for facultative cheating and kin selection in the evolution of quorum-sensing diversity.social evolution | sociomicrobiology | Bacillus subtilis | bacteria | quorum sensing I n many bacteria, a cell-cell signaling mechanism, known as quorum sensing, coordinates the response of a bacterial community in a density-dependent manner. Quorum-sensing bacteria secrete a signal molecule known as an autoinducer and express a specific receptor that binds to it with high affinity, resulting in the activation of a specific cellular response (1). Quorum sensing often regulates the secretion of public goods or other cooperative traits that benefit the community, at a cost to the individual responding cell (2).The regulation of cooperation by a secreted autoinducer allows for the evolution of cheater genotypes that do not produce the autoinducer or do not respond to it (3, 4). Mutants of the latter type were shown to act as cheaters in a variety of different species (3-7). The elimination of these cheater mutants could occur by kin selection, where cooperation is preferentially directed toward other cooperators (3,(7)(8)(9).In contrast to the rarity of quorum-sensing response null alleles in wild populations, many species display a high degree of intraspecific genetic variation in functional quorum-sensing alleles, called pherotypes (Fig. 1A). Each allele codes for both receptor and autoinducer genes, where an autoinducer coded by one pherotype will activate its coencoded receptor, but not the receptors encoded by other pherotypes (10-14). Pherotypes differ in their receptor-autoinducer specificity but not in the pathways regulated by the receptor. In addition, many pherotypes show patterns of intraspecific horizontal gene transfer (10, 12) and coexist in the same environment (15, 16).The mechanisms that lead to the diversification of pherotypes, to the maintenance of their diversity, and to their rapid horizontal gene transfer are not well understood. We have previously proposed, by analyzing a theoretical model, that if quorum sensing regulates cooperation, novel pherotypes can arise adaptivel...