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Quorum sensing as a mechanism to harness the wisdom of the crowds.

ABSTRACT: Bacteria release and sense small molecules called autoinducers in a process known as quorum sensing. The prevailing interpretation of quorum sensing is that by sensing autoinducer concentrations, bacteria estimate population density to regulate the expression of functions that are only beneficial when carried out by a sufficiently large number of cells. However, a major challenge to this interpretation is that the concentration of autoinducers strongly depends on the environment, often rendering autoinducer-based estimates of cell density unreliable. Here we propose an alternative interpretation of quorum sensing, where bacteria, by releasing and sensing autoinducers, harness social interactions to sense the environment as a collective. Using a computational model we show that this functionality can explain the evolution of quorum sensing and arises from individuals improving their estimation accuracy by pooling many imperfect estimates - analogous to the 'wisdom of the crowds' in decision theory. Importantly, our model reconciles the observed dependence of quorum sensing on both population density and the environment and explains why several quorum sensing systems regulate the production of private goods.

SUBMITTER: Moreno-Gamez S

PROVIDER: S-EPMC10256802 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Quorum sensing as a mechanism to harness the wisdom of the crowds.

Moreno-Gámez Stefany S Hochberg Michael E ME van Doorn G S GS

Nature communications 20230609 1

Bacteria release and sense small molecules called autoinducers in a process known as quorum sensing. The prevailing interpretation of quorum sensing is that by sensing autoinducer concentrations, bacteria estimate population density to regulate the expression of functions that are only beneficial when carried out by a sufficiently large number of cells. However, a major challenge to this interpretation is that the concentration of autoinducers strongly depends on the environment, often rendering ...[more]

PMID: 37296108

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Project description:One of the key determinants of the size, composition, structure, and development of a microbial community is the predation pressure by bacteriophages. Accordingly, bacteria have evolved a battery of antiphage defense strategies. Since maintaining constantly elevated defenses is costly, we hypothesize that some bacteria have additionally evolved the abilities to estimate the risk of phage infection and to adjust their strategies accordingly. One risk parameter is the density of the bacterial population. Hence, quorum sensing, i.e., the ability to regulate gene expression according to population density, may be an important determinant of phage-host interactions. This hypothesis was investigated in the model system of Escherichia coli and phage ?. We found that, indeed, quorum sensing constitutes a significant, but so far overlooked, determinant of host susceptibility to phage attack. Specifically, E. coli reduces the numbers of ? receptors on the cell surface in response to N-acyl-l-homoserine lactone (AHL) quorum-sensing signals, causing a 2-fold reduction in the phage adsorption rate. The modest reduction in phage adsorption rate leads to a dramatic increase in the frequency of uninfected survivor cells after a potent attack by virulent phages. Notably, this mechanism may apply to a broader range of phages, as AHLs also reduce the risk of ? phage infection through a different receptor. IMPORTANCE To enable the successful manipulation of bacterial populations, a comprehensive understanding of the factors that naturally shape microbial communities is required. One of the key factors in this context is the interactions between bacteria and the most abundant biological entities on Earth, namely, the bacteriophages that prey on bacteria. This proof-of-principle study shows that quorum sensing plays an important role in determining the susceptibility of E. coli to infection by bacteriophages ? and ?. On the basis of our findings in the classical Escherichia coli-? model system, we suggest that quorum sensing may serve as a general strategy to protect bacteria specifically under conditions of high risk of infection.

Dataset Information

Quorum sensing as a mechanism to harness the wisdom of the crowds.

Publications

Quorum sensing as a mechanism to harness the wisdom of the crowds.

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