Experimental Evolution of Anticipatory Regulation in Escherichia coli.

Anjali Mahilkar,Akshat Mall,Supreet Saini,Pavithra Venkataraman

doi:10.3389/fmicb.2021.796228

Anjali Mahilkar, Akshat Mall + Show 2 more

Open Access

https://doi.org/10.3389/fmicb.2021.796228

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Abstract

Environmental cues in an ecological niche are often temporal in nature. For instance, in temperate climates, temperature is higher in daytime compared to during night. In response to these temporal cues, bacteria have been known to exhibit anticipatory regulation, whereby triggering response to a yet to appear cue. Such an anticipatory response in known to enhance Darwinian fitness, and hence, is likely an important feature of regulatory networks in microorganisms. However, the conditions under which an anticipatory response evolves as an adaptive response are not known. In this work, we develop a quantitative model to study response of a population to two temporal environmental cues, and predict variables which are likely important for evolution of anticipatory regulatory response. We follow this with experimental evolution of Escherichia coli in alternating environments of rhamnose and paraquat for ∼850 generations. We demonstrate that growth in this cyclical environment leads to evolution of anticipatory regulation. As a result, pre-exposure to rhamnose leads to a greater fitness in paraquat environment. Genome sequencing reveals that this anticipatory regulation is encoded via mutations in global regulators. Overall, our study contributes to understanding of how environment shapes the topology of regulatory networks in an organism.

Highlights

Environmental cues are often cyclical in nature, for instance, temperature in day is higher and night is cooler
Because of cyclic AMP receptor protein (CRP)-cAMP complex has a global affect on gene regulation, the gene expression patterns in the cell in a cya mutant are qualitatively different, compared to the wild-type (Delaney, 1990)
While the mechanistic explanation for the observed anticipatory regulation, and the corresponding increase in fitness is difficult to understand fully from the sequencing results, our results demonstrate how small mutations in global regulators of a cell can bring about fine-tuning of gene expression which leads to changes in timing and strength of gene expression, contributing to cellular fitness

Summary

INTRODUCTION

Environmental cues are often cyclical in nature, for instance, temperature in day is higher and night is cooler. In Escherichia coli, an increase in temperature elicits response to low oxygen conditions, mimicking how these two environments are sequentially encountered by the bacterium in the mammalian gastrointestinal tract (Tagkopoulos et al, 2008) Such anticipatory regulation was demonstrated to occur between sugars lactose and maltose (Mitchell et al, 2009). Repeated, alternating exposure to S1 and S2 for ∼850 generations, leads to evolution of anticipatory regulation, where prior exposure to rhamnose provides an adaptive benefit when the population is shifted to paraquat This benefit is observed only in lines, which were exposed to alternating S1 and S2; and is only seen when these cells are pre-exposed to rhamnose. Genome sequencing of the evolved lines reveals that anticipatory regulation can evolve via distinct molecular pathways, often involving mutations in global regulators

MATERIALS AND METHODS

RESULTS

DISCUSSION AND CONCLUSION

DATA AVAILABILITY STATEMENT