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Poor sensing maximises microbial fitness when few out of many signals are sensed

By Age J. Tjalma, Robert Planque, Frank J. Bruggeman

Posted 10 Oct 2019
bioRxiv DOI: 10.1101/800292

An open problem in biology is to understand when particular adaptation strategies of microorganisms are selected during evolution. They range from random, bet-hedging strategies to deterministic, responsive strategies, relying on signalling circuits. We present an evolutionary model that integrates basic statistical physics of molecular circuits with fitness maximisation and information theory. This model provides an explanation for a puzzling observation on responsive strategies: the accuracy with which signalling networks track external signals seems remarkably low. Single cells often distinguish only between 2 to 4 concentration ranges, corresponding to 1 or 2 bits of mutual information between signal and response. Why did evolution lead to such low-fidelity signalling systems? Our theory offers an explanation by taking a novel perspective. It considers the fitness benefit of all signals, including those that are not sensed. We introduce a new concept, `latent information', which captures the mutual information between all non-sensed signals and the optimal response. The theory predicts that it is often evolutionarily optimal to transduce sensed signals noisily when latent information is present. It indicates that fitness can indeed be maximal when the mutual information extracted from sensed signals is not maximal, but rather has a low value of about 1 or 2 bits. Cells likely do not sense all signals because of the fitness cost of expressing idle signalling systems that consume limited biosynthetic resources. Our theory illustrates that as the total available information about the optimal behaviour decreases, the cell should trust the available information less, and gamble more.

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