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A reversible mutation in a genomic hotspot saves bacterial swarms from extinction.

ABSTRACT: Microbial adaptation to changing environmental conditions is frequently mediated by hypermutable sequences. Here we demonstrate that such a hypermutable hotspot within a gene encoding a flagellar unit of Paenibacillus glucanolyticus generated spontaneous non-swarming mutants with increased stress resistance. These mutants, which survived conditions that eliminated wild-type cultures, could be carried by their swarming siblings when the colony spread, consequently increasing their numbers at the spreading edge. Of interest, the hypermutable nature of the aforementioned sequence enabled the non-swarming mutants to serve as "seeds" for a new generation of wild-type cells through reversion of the mutation. Using a mathematical model, we examined the survival dynamics of P. glucanolyticus colonies under fluctuating environments. Our experimental and theoretical results suggest that the non-swarming, stress-resistant mutants can save the colony from extinction. Notably, we identified this hypermutable sequence in flagellar genes of additional Paenibacillus species, suggesting that this phenomenon could be wide-spread and ecologically important.

SUBMITTER: Hefetz I

PROVIDER: S-EPMC9941203 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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A reversible mutation in a genomic hotspot saves bacterial swarms from extinction.

Hefetz Idan I Israeli Ofir O Bilinsky Gal G Plaschkes Inbar I Hazkani-Covo Einat E Hayouka Zvi Z Lampert Adam A Helman Yael Y

iScience 20230125 2

Microbial adaptation to changing environmental conditions is frequently mediated by hypermutable sequences. Here we demonstrate that such a hypermutable hotspot within a gene encoding a flagellar unit of <i>Paenibacillus glucanolyticus</i> generated spontaneous non-swarming mutants with increased stress resistance. These mutants, which survived conditions that eliminated wild-type cultures, could be carried by their swarming siblings when the colony spread, consequently increasing their numbers ...[more]

PMID: 36824284

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Project description:It is widely recognized that we are entering an extinction event on a scale approaching the mass extinctions seen in the fossil record. Present-day rates of extinction are estimated to be several orders of magnitude greater than background rates and are projected to increase further if current trends continue. In vertebrates, species traits, such as body size, fecundity, and geographic range, are important predictors of vulnerability. Although plants are the basis for life on Earth, our knowledge of plant extinctions and vulnerabilities is lagging. Here, we disentangle the underlying drivers of extinction risk in plants, focusing on the Cape of South Africa, a global biodiversity hotspot. By comparing Red List data for the British and South African floras, we demonstrate that the taxonomic distribution of extinction risk differs significantly between regions, inconsistent with a simple, trait-based model of extinction. Using a comprehensive phylogenetic tree for the Cape, we reveal a phylogenetic signal in the distribution of plant extinction risks but show that the most threatened species cluster within short branches at the tips of the phylogeny--opposite to trends in mammals. From analyzing the distribution of threatened species across 11 exemplar clades, we suggest that mode of speciation best explains the unusual phylogenetic structure of extinction risks in plants of the Cape. Our results demonstrate that explanations for elevated extinction risk in plants of the Cape flora differ dramatically from those recognized for vertebrates. In the Cape, extinction risk is higher for young and fast-evolving plant lineages and cannot be explained by correlations with simple biological traits. Critically, we find that the most vulnerable plant species are nonetheless marching towards extinction at a more rapid pace but, surprisingly, independently from anthropogenic effects. Our results have important implications for conservation priorities and cast doubts on the utility of current Red List criteria for plants in regions such as the Cape, where speciation has been rapid, if our aim is to maximize the preservation of the tree-of-life.

Project description:UNLABELLED:Swarming bacteria are challenged by the need to invade hostile environments. Swarms of the flagellated bacterium Paenibacillus vortex can collectively transport other microorganisms. Here we show that P. vortex can invade toxic environments by carrying antibiotic-degrading bacteria; this transport is mediated by a specialized, phenotypic subpopulation utilizing a process not dependent on cargo motility. Swarms of beta-lactam antibiotic (BLA)-sensitive P. vortex used beta-lactamase-producing, resistant, cargo bacteria to detoxify BLAs in their path. In the presence of BLAs, both transporter and cargo bacteria gained from this temporary cooperation; there was a positive correlation between BLA resistance and dispersal. P. vortex transported only the most beneficial antibiotic-resistant cargo (including environmental and clinical isolates) in a sustained way. P. vortex displayed a bet-hedging strategy that promoted the colonization of nontoxic niches by P. vortex alone; when detoxifying cargo bacteria were not needed, they were lost. This work has relevance for the dispersal of antibiotic-resistant microorganisms and for strategies for asymmetric cooperation with agricultural and medical implications. IMPORTANCE:Antibiotic resistance is a major health threat. We show a novel mechanism for the local spread of antibiotic resistance. This involves interactions between different bacteria: one species provides an enzyme that detoxifies the antibiotic (a sessile cargo bacterium carrying a resistance gene), while the other (Paenibacillus vortex) moves itself and transports the cargo. P. vortex used a bet-hedging strategy, colonizing new environments alone when the cargo added no benefit, but cooperating when the cargo was needed. This work is of interest in an evolutionary context and sheds light on fundamental questions, such as how environmental antibiotic resistance may lead to clinical resistance and also microbial social organization, as well as the costs, benefits, and risks of dispersal in the environment.

Dataset Information

A reversible mutation in a genomic hotspot saves bacterial swarms from extinction.

Publications

A reversible mutation in a genomic hotspot saves bacterial swarms from extinction.

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