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Transition to quorum sensing in an Agrobacterium population: A stochastic model.

ABSTRACT: Understanding of the intracellular molecular machinery that is responsible for the complex collective behavior of multicellular populations is an exigent problem of modern biology. Quorum sensing, which allows bacteria to activate genetic programs cooperatively, provides an instructive and tractable example illuminating the causal relationships between the molecular organization of gene networks and the complex phenotypes they control. In this work we--to our knowledge for the first time--present a detailed model of the population-wide transition to quorum sensing using the example of Agrobacterium tumefaciens. We construct a model describing the Ti plasmid quorum-sensing gene network and demonstrate that it behaves as an "on-off" gene expression switch that is robust to molecular noise and that activates the plasmid conjugation program in response to the increase in autoinducer concentration. This intracellular model is then incorporated into an agent-based stochastic population model that also describes bacterial motion, cell division, and chemical communication. Simulating the transition to quorum sensing in a liquid medium and biofilm, we explain the experimentally observed gradual manifestation of the quorum-sensing phenotype by showing that the transition of individual model cells into the "on" state is spread stochastically over a broad range of autoinducer concentrations. At the same time, the population-averaged values of critical autoinducer concentration and the threshold population density are shown to be robust to variability between individual cells, predictable and specific to particular growth conditions. Our modeling approach connects intracellular and population scales of the quorum-sensing phenomenon and provides plausible answers to the long-standing questions regarding the ecological and evolutionary significance of the phenomenon. Thus, we demonstrate that the transition to quorum sensing requires a much higher threshold cell density in liquid medium than in biofilm, and on this basis we hypothesize that in Agrobacterium quorum sensing serves as the detector of biofilm formation.

SUBMITTER: Goryachev AB

PROVIDER: S-EPMC1214540 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundA wide range of bacteria species are known to communicate through the so called quorum sensing (QS) mechanism by means of which they produce a small molecule that can freely diffuse in the environment and in the cells. Upon reaching a threshold concentration, the signalling molecule activates the QS-controlled genes that promote phenotypic changes. This mechanism, for its simplicity, has become the model system for studying the emergence of a global response in prokaryotic cells. Yet, how cells precisely measure the signal concentration and act coordinately, despite the presence of fluctuations that unavoidably affects cell regulation and signalling, remains unclear.ResultsWe propose a model for the QS signalling mechanism in Vibrio fischeri based on the synthetic strains lux01 and lux02. Our approach takes into account the key regulatory interactions between LuxR and LuxI, the autoinducer transport, the cellular growth and the division dynamics. By using both deterministic and stochastic models, we analyze the response and dynamics at the single-cell level and compare them to the global response at the population level. Our results show how fluctuations interfere with the synchronization of the cell activation and lead to a bimodal phenotypic distribution. In this context, we introduce the concept of precision in order to characterize the reliability of the QS communication process in the colony. We show that increasing the noise in the expression of LuxR helps cells to get activated at lower autoinducer concentrations but, at the same time, slows down the global response. The precision of the QS switch under non-stationary conditions decreases with noise, while at steady-state it is independent of the noise value.ConclusionsOur in silico experiments show that the response of the LuxR/LuxI system depends on the interplay between non-stationary and stochastic effects and that the burst size of the transcription/translation noise at the level of LuxR controls the phenotypic variability of the population. These results, together with recent experimental evidences on LuxR regulation in wild-type species, suggest that bacteria have evolved mechanisms to regulate the intensity of those fluctuations.

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Transition to quorum sensing in an Agrobacterium population: A stochastic model.

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