Abstract
Understanding the principles underlying the plasticity of signal transduction networks is fundamental to decipher the functioning of living cells. In Myxococcus xanthus, a particular chemosensory system (Frz) coordinates the activity of two separate motility systems (the A- and S-motility systems), promoting multicellular development. This unusual structure asks how signal is transduced in a branched signal transduction pathway. Using combined evolution-guided and single cell approaches, we successfully uncoupled the regulations and showed that the A-motility regulation system branched-off an existing signaling system that initially only controlled S-motility. Pathway branching emerged in part following a gene duplication event and changes in the circuit structure increasing the signaling efficiency. In the evolved pathway, the Frz histidine kinase generates a steep biphasic response to increasing external stimulations, which is essential for signal partitioning to the motility systems. We further show that this behavior results from the action of two accessory response regulator proteins that act independently to filter and amplify signals from the upstream kinase. Thus, signal amplification loops may underlie the emergence of new connectivity in signal transduction pathways.
Highlights
In living cells, adaptation to rapid changes in environmental conditions requires coordinated rearrangements of basic cellular processes to adjust the cellular homeostasis to the new conditions
While Tfp systems are found in all deltaproteobacterial genomes [26,35], the A-motility Agl-Glt machinery is only present in Cystobacterineae, a Deltaproteobacteria family [15,16,36]
S-motility may be more ancient than A-motility and the emergence of A-motility in Cystobacterineae could have expanded the phenotypic repertoire and adaptive capabilities of this family of bacteria
Summary
Adaptation to rapid changes in environmental conditions requires coordinated rearrangements of basic cellular processes to adjust the cellular homeostasis to the new conditions. Receptor molecules sense environmental changes and translate them into a cellular response by phosphorylation of a downstream regulator. Because the cellular response must be integrated to various cellular processes, the phosphorylation cascade frequently involves a number of intermediates, allowing multiple regulation layers and branch points (nodes) in the regulatory circuit [1,2]. For a given pathway, identifying nodes and understanding how they participate in the regulation is of fundamental importance to elucidate how signals are integrated toward a cellular response. Some proteins that appear central to the regulation in a given genetic context may be dispensable in a different context where their function is not required. Bacteria are exceptional model systems for such studies because they are highly tractable experimentally and thousands of genome have been sequenced
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