Ratiometric population sensing by a pump-probe signaling system in Bacillus subtilis

Babel, Heiko; Naranjo-Meneses, Pablo; Trauth, Stephanie; Schulmeister, Sonja; Malengo, Gabriele; Sourjik, Victor; Bischofs, Ilka B.

doi:10.1038/s41467-020-14840-w

Cited by 21 publications

(24 citation statements)

References 69 publications

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“…Ratiometric sensing was recently described for other binary populations, such as those composed of signal producers and signal “cheaters” in the PhrA-RapA-Spo0F signaling pathway in Bacillus subtilis [ 26 ] and yeast mating types [ 24 ]. In both cases, ratiometric sensing is achieved by cell density–dependent reductions in extracellular signal availability.…”

Section: Discussionmentioning

confidence: 99%

Ratiometric quorum sensing governs the trade-off between bacterial vertical and horizontal antibiotic resistance propagation

et al. 2020

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Plasmid-mediated horizontal gene transfer of antibiotic resistance and virulence in pathogenic bacteria underlies a major public health issue. Understanding how, in the absence of antibiotic-mediated selection, plasmid-bearing cells avoid being outnumbered by plasmid-free cells is key to developing counterstrategies. Here, we quantified the induction of the plasmidial sex pheromone pathway of Enterococcus faecalis to show that the integration of the stimulatory (mate-sensing) and inhibitory (self-sensing) signaling modules from the pCF10 conjugative plasmid provides a precise measure of the recipient-to-donor ratio, agnostic to variations in population size. Such ratiometric control of conjugation favors vertical plasmid transfer under low mating likelihood and allows activation of conjugation functions only under high mating likelihood. We further show that this strategy constitutes a cost-effective investment into mating effort because overstimulation produces unproductive self-aggregation and growth rate reduction. A mathematical model suggests that ratiometric control of conjugation increases plasmid fitness and predicts a robust long-term, stable coexistence of donors and recipients. Our results demonstrate how population-level parameters can control transfer of antibiotic resistance in bacteria, opening the door for biotic control strategies.

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Section: Discussionmentioning

confidence: 99%

Ratiometric quorum sensing governs the trade-off between bacterial vertical and horizontal antibiotic resistance propagation

et al. 2020

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“…Ideally, every cell produces signaling molecules, shares signaling molecules, and coordinately responds to the signaling molecules. In recent years, however, it was shown that the expression of signaling molecules can be heterogenous [23][24][25][26] . When the concentration of signaling molecule reaches a threshold value, a coordinated and homogeneous expression of target genes may be initiated in all cells of the population 5,27 or a heterogeneous gene expression in the population may be triggered at low concentrations 25,27,28 .…”

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confidence: 99%

Peptide signaling without feedback in signal production operates as a true quorum sensing communication system in Bacillus subtilis

et al. 2021

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Bacterial quorum sensing (QS) is based on signal molecules (SM), which increase in concentration with cell density. At critical SM concentration, a variety of adaptive genes sharply change their expression from basic level to maximum level. In general, this sharp transition, a hallmark of true QS, requires an SM dependent positive feedback loop, where SM enhances its own production. Some communication systems, like the peptide SM-based ComQXPA communication system of Bacillus subtilis, do not have this feedback loop and we do not understand how and if the sharp transition in gene expression is achieved. Based on experiments and mathematical modeling, we observed that the SM peptide ComX encodes the information about cell density, specific cell growth rate, and even oxygen concentration, which ensure power-law increase in SM production. This enables together with the cooperative response to SM (ComX) a sharp transition in gene expression level and this without the SM dependent feedback loop. Due to its ultra-sensitive nature, the ComQXPA can operate at SM concentrations that are 100–1000 times lower than typically found in other QS systems, thereby substantially reducing the total metabolic cost of otherwise expensive ComX peptide.

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“…Based on comparison of the sizes and integration sites of prophage elements within Bacillus sp., SPβ and phi3T clearly belong to a distinct prophage group. These phages appear extremely large (2-3-fold larger than average prophages), and they possess sophisticated communication systems that are potentially capable of sensing the frequency of lysogenized hosts [64, 87] or biosynthetic gene clusters [88, 89], and functional genes related to host dormancy [90, 91]. A high level of homology between SPβ and phi3Ts offers extensive regions for homologous recombination, which can be additionally promoted by the recombination machinery involved in natural competence [92] and in non-homologous end-joining repair [93].…”

Section: Discussionmentioning

confidence: 99%

Pervasive prophage recombination occurs during evolution of spore-formingBacilli

Dragoš

Priyadarshini

Hasan

et al. 2020

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24Phages are the main source of within-species bacterial diversity and drivers of horizontal gene 25 transfer. Prophage cargo can determine ecological interactions of a bacterium with other 26 community members, and even its pathogenic potential, but we know little about the 27 mechanisms that drive genetic diversity of these mobile genetic elements (MGEs). Recently, 28 we showed that a sporulation selection regime promotes evolutionary changes within SPβ 29 prophage of Bacillus subtilis, leading to direct antagonistic interactions within the population. 30 Interestingly, SPβ belongs to the so-called phage regulatory switches that precisely excise from 31 the chromosome of sporulating mother cells, a phenomenon observed for phages infecting 32 diverse spore-forming species. Herein, we reveal that under a sporulation selection regime, SPβ 33 recombines with low copy number phi3Ts phage DNA present within the B. subtilis population. 34Recombination results in a new prophage occupying a different integration site, as well as the 35 spontaneous release of virulent phage hybrids. Analysis of Bacillus sp. strains suggests that 36 SPβ and phi3T belong to a distinct cluster of unusually large phages inserted into sporulation-37 related genes that are equipped with a spore-related genetic arsenal. Comparison of Bacillus 38 sp. genomes at global and local ecological scales indicates that these SPβ-like phages diversify 39 rapidly, especially in the absence of other MGEs constraining their lytic cycle. Our study 40 captures inter-phage recombination under an experimentally imposed selection regime, and 41 reveals the ubiquity of similar phenomena in Bacillus sp. genomic data. Therefore, our work is 42 a stepping stone toward empirical studies on phage evolution, and understanding the eco-43 evolutionary relationships between bacteria and their phages.44 45 46 47 72 4 specialised 21,22 transduction, respectively, thereby contributing to the spread of antibiotic 73 resistance 20 or virulence genes 23 . Although evidence from comparative phage genomics 74 indicates frequent recombination into new phage variants (so-called gene shuffling) 13,24,25 , this 75 is not reflected in experimental research. Phage recombination has been experimentally studied 76 using limited models, predominantly Salmonella typhimurium P22 with Escherichia coli 77 lambdoid phages 26,27 . Therefore, despite our knowledge of pronounced genomic mosaicism, 78 empirical research on prophage evolution is relatively limited. Combining such research with 79 broader comparisons of available host genomes may prove key to understanding the ecology 80 and evolution of bacteria and phages, including whether prophages serve as a major source of 81 bacterial within-species diversity, or as regulators. 82 Interestingly, certain prophages of Bacilli undergo genetic rearrangements upon 83 host development, acting as so-called phage regulatory switches (RSs) 28 . RS phages can switch 84 between integrated and extrachromosomal forms to modulate reproduction and surv...

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Ratiometric population sensing by a pump-probe signaling system in Bacillus subtilis

Cited by 21 publications

References 69 publications

Ratiometric quorum sensing governs the trade-off between bacterial vertical and horizontal antibiotic resistance propagation

Ratiometric quorum sensing governs the trade-off between bacterial vertical and horizontal antibiotic resistance propagation

Peptide signaling without feedback in signal production operates as a true quorum sensing communication system in Bacillus subtilis

Pervasive prophage recombination occurs during evolution of spore-formingBacilli

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