Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis.
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ABSTRACT:
SUBMITTER: Stefanic P
PROVIDER: S-EPMC8187645 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description: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.
| S-EPMC4653157 | biostudies-literature
Project description:Multicellularity inherently involves a number of cooperative behaviors that are potentially susceptible to exploitation but can be protected by mechanisms such as kin discrimination. Discrimination of kin from non-kin has been observed in swarms of the bacterium Bacillus subtilis, but the underlying molecular mechanism has been unknown. We used genetic, transcriptomic, and bioinformatic analyses to uncover kin recognition factors in this organism. Our results identified many molecules involved in cell-surface modification and antimicrobial production and response. These genes varied significantly in expression level and mutation phenotype among B. subtilis strains, suggesting interstrain variation in the exact kin discrimination mechanism used. Genome analyses revealed a substantial diversity of antimicrobial genes present in unique combinations in different strains, with many likely acquired by horizontal gene transfer. The dynamic combinatorial effect derived from this plethora of kin discrimination genes creates a tight relatedness cutoff for cooperation that has likely led to rapid diversification within the species. Our data suggest that genes likely originally selected for competitive purposes also generate preferential interactions among kin, thus stabilizing multicellular lifestyles.
| S-EPMC4803606 | biostudies-literature
Project description:Swarming is the collective movement of bacteria across a surface. It requires the production of surfactants (public goods) to overcome surface tension and provides an excellent model to investigate bacterial cooperation. Previously, we correlated swarm interaction phenotypes with kin discrimination between B. subtilis soil isolates, by showing that less related strains form boundaries between swarms and highly related strains merge. However, how kin discrimination affects cooperation and territoriality in swarming bacteria remains little explored. Here we show that the pattern of surface colonization by swarming mixtures is influenced by kin types. Closely related strain mixtures colonize the surface in a mixed swarm, while mixtures of less related strains show competitive exclusion as only one strain colonizes the surface. The outcome of nonkin swarm expansion depends on the initial ratio of the competing strains, indicating positive frequency-dependent competition. We find that addition of surfactin (a public good excreted from cells) can complement the swarming defect of nonkin mutants, whereas close encounters in nonkin mixtures lead to territorial exclusion, which limits the exploitation of surfactin by nonkin nonproducers. The work suggests that kin discrimination driven competitive territorial exclusion may be an important determinant for the success of cooperative surface colonization.
| S-EPMC8857193 | biostudies-literature
Project description:Kin discrimination in nature is an effective way for bacteria to stabilize population cooperation and maintain progeny benefits. However, so far, the research on kin discrimination for Bacillus still has concentrated on "attack and defense" between cells and diffusion-dependent molecular signals of quorum sensing, kin recognition in Bacillus, however, has not been reported. To determine whether flagellar is involve in the kin recognition of Bacillus, we constructed Bacillus velezensis SQR9 assembled with flagellin of its kin and non-kin strains, and performed a swarm boundary assay with SQR9, then analyzed sequence variation of flagellin and other flagellar structural proteins in B. velezensis genus. Our results showed that SQR9 assembled with flagellin of non-kin strains was more likely to form a border phenotype with wild-type strain SQR9 in swarm assay than that of kin strains, and that non-kin strains had greater variation in flagellin than kin strains. In B. velezensis, these variations in flagellin were prevalent and had evolved significantly faster than other flagellar structural proteins. Therefore, we proposed that flagellin is an effective tool partly involved in the kin recognition of B. velezensis strains. IMPORTANCE Kin selection plays an important role in stabilizing population cooperation and maintaining the progeny benefits for bacteria in nature. However, to date, the role of flagellin in kin recognition in Bacillus has not been reported. By using rhizospheric Bacillus velezensis SQR9, we accomplished flagellin region interchange among its related strains, and show that flagellin acts as a mediator to distinguish kin from non-kin in B. velezensis. We demonstrated the polymorphism of flagellin in B. velezensis through alignment analysis of flagellin protein sequences. Therefore, it was proposed that flagellin was likely to be an effective tool for mediating kin recognition in B. velezensis.
| S-EPMC9764977 | biostudies-literature
Project description:Cytological and genetic evidence suggests that the Bacillus subtilis DNA uptake machinery localizes at a single cell pole and takes up single-stranded (ss) DNA. The integration of homologous donor DNA into the recipient chromosome requires RecA, while plasmid establishment, which is independent of RecA, requires at least RecO and RecU. RecA and RecN colocalize at the polar DNA uptake machinery, from which RecA forms filamentous structures, termed threads, in the presence of chromosomal DNA. We show that the transformation of chromosomal and of plasmid DNA follows distinct pathways. In the absence of DNA, RecU accumulated at a single cell pole in competent cells, dependent on RecA. Upon addition of any kind of DNA, RecA formed highly dynamic thread structures, which rapidly grew and shrank, and RecU dissipated from the pole. RecO visibly accumulated at the cell pole only upon addition of plasmid DNA, and, to a lesser degree, of phage DNA, but not of chromosomal DNA. RecO accumulation was weakly influenced by RecN, but not by RecA. RecO annealed ssDNA complexed with SsbA in vitro, independent of any nucleotide cofactor. The DNA end-joining Ku protein was also found to play a role in viral and plasmid transformation. On the other hand, transfection with SPP1 phage DNA required functions from both chromosomal and plasmid transformation pathways. The findings show that competent bacterial cells possess a dynamic DNA recombination machinery that responds in a differential manner depending if entering DNA shows homology with recipient DNA or has self-annealing potential. Transformation with chromosomal DNA only requires RecA, which forms dynamic filamentous structures that may mediate homology search and DNA strand invasion. Establishment of circular plasmid DNA requires accumulation of RecO at the competence pole, most likely mediating single-strand annealing, and RecU, which possibly down-regulates RecA. Transfection with SPP1 viral DNA follows an intermediate route that contains functions from both chromosomal and plasmid transformation pathways.
| S-EPMC2727465 | biostudies-literature
Project description:Background: Wall teichoic acid (WTA) genes are essential for production of cell walls in gram-positive bacteria and necessary for survival and variability in the cassette has led to recent antibiotic resistance acquisition in pathogenic bacteria. Methods: Using a pan-genome approach, we examined the evolutionary history of WTA genes in Bacillus subtilis ssp. subtilis. Results: Our analysis reveals an interesting pattern of evolution from the type-strain WTA gene cassette possibly resulting from horizontal acquisition from organisms with similar gene sequences. The WTA cassettes have a high level of variation which may be due to one or more independent horizontal transfer events during the evolution of Bacillus subtilis ssp. subtilis. This swapping of entire WTA cassettes and smaller regions within the WTA cassettes is an unusual feature in the evolution of the Bacillus subtilis genome and highlights the importance of horizontal transfer of gene cassettes through homologous recombination within B. subtilis or other bacterial species. Conclusions: Reduced sequence conservation of these WTA cassettes may indicate a modified function like the previously documented WTA ribitol/glycerol variation. An improved understanding of high-frequency recombination of gene cassettes has ramifications for synthetic biology and the use of B. subtilis in industry.
| S-EPMC8753576 | biostudies-literature
Project description:Iturin A and its derivatives are lipopeptide antibiotics produced by Bacillus subtilis and several closely related bacteria. Three iturin group operons (i.e., iturin A, mycosubtilin, and bacillomycin D) of those antibiotic-producing strains have been cloned and sequenced thus far, strongly implying the horizontal transfer of these operons. To examine the nature of such horizontal transfer in terms of antibiotic production, a 42-kb region of the B. subtilis RB14 genome, which contains a complete 38-kb iturin A operon, was transferred via competent cell transformation to the genome of a non-iturin A producer, B. subtilis 168, using a method based on double-crossover homologous recombination with two short landing pad sequences (LPSs) in the genome. The recombinant was positively selected by confirming the elimination of the cI repressor gene, which was localized between the two LPSs and substituted by the transferred segment. The iturin A operon-transferred strain 168 was then converted into an iturin A producer by the introduction of an sfp gene, which encodes 4'-phosphopantetheinyl transferase and is mutated in strain 168. By inserting the pleiotropic regulator degQ, the productivity of iturin A increased sevenfold and was restored to about half that of the donor strain RB14, without the transfer of additional genes, such as regulatory or self-resistance genes.
| S-EPMC1280175 | biostudies-literature
Project description:Laboratory experiments have suggested that bacteria perform a range of cooperative behaviors, which are favored because they are directed toward relatives (kin selection). However, there is a lack of evidence for cooperation and kin selection in natural bacterial populations. Molecular population genetics offers a promising method to study natural populations because the theory predicts that kin selection will lead to relaxed selection, which will result in increased polymorphism and divergence at cooperative genes. Examining a natural population of Bacillus subtilis, we found consistent evidence that putatively cooperative traits have higher polymorphism and greater divergence than putatively private traits expressed at the same rate. In addition, we were able to eliminate alternative explanations for these patterns and found more deleterious mutations in genes controlling putatively cooperative traits. Overall, our results suggest that cooperation is favored by kin selection, with an average relatedness of r = .79 between interacting individuals.
| S-EPMC10565896 | biostudies-literature
Project description:Tracing evolutionary processes that lead to fixation of genomic variation in wild bacterial populations is a prime challenge in molecular evolution. In particular, the relative contribution of horizontal gene transfer (HGT) vs. de novo mutations during adaptation to a new environment is poorly understood. To gain a better understanding of the dynamics of HGT and its effect on adaptation, we subjected several populations of competent Bacillus subtilis to a serial dilution evolution on a high-salt-containing medium, either with or without foreign DNA from diverse pre-adapted or naturally salt tolerant species. Following 504 generations of evolution, all populations improved growth yield on the medium. Sequencing of evolved populations revealed extensive acquisition of foreign DNA from close Bacillus donors but not from more remote donors. HGT occurred in bursts, whereby a single bacterial cell appears to have acquired dozens of fragments at once. In the largest burst, close to 2% of the genome has been replaced by HGT. Acquired segments tend to be clustered in integration hotspots. Other than HGT, genomes also acquired spontaneous mutations. Many of these mutations occurred within, and seem to alter, the sequence of flagellar proteins. Finally, we show that, while some HGT fragments could be neutral, others are adaptive and accelerate evolution.
| S-EPMC7536860 | biostudies-literature
Project description:Genetic relatedness is a key driver of the evolution of cooperation. One mechanism that may ensure social partners are genetically related is kin discrimination, in which individuals are able to distinguish kin from non-kin and adjust their behaviour accordingly. However, the impact of kin discrimination upon the overall level of cooperation remains obscure. Specifically, while kin discrimination allows an individual to help more-related social partners over less-related social partners, it is unclear whether and how the population average level of cooperation that is evolutionarily favoured should differ under kin discrimination versus indiscriminate social behaviour. Here, we perform a general mathematical analysis in order to assess whether, when and in which direction kin discrimination changes the average level of cooperation in an evolving population. We find that kin discrimination may increase, decrease or leave unchanged the average level of cooperation, depending upon whether the optimal level of cooperation is a convex, concave or linear function of genetic relatedness. We develop an extension of the classic 'tragedy of the commons' model of cooperation in order to provide an illustration of these results. Our analysis provides a method to guide future research on the evolutionary consequences of kin discrimination.
| S-EPMC7115181 | biostudies-literature