REC protein family expansion by the emergence of a new signaling pathway

Garber, Megan E.; Frank, Vered; Kazakov, Alexey E.; Incha, Matthew R.; Nava, Alberto A.; Zhang, Hanqiao; Valencia, Luis E.; Keasling, Jay D.; Rajeev, Lara; Mukhopadhyay, Aindrila

doi:10.1128/mbio.02622-23

Title: REC protein family expansion by the emergence of a new signaling pathway

Journal Article · 22 November 2023 · mBio (Online)

DOI: https://doi.org/10.1128/mbio.02622-23 · OSTI ID:2221817

^[1]; Frank, Vered ^[2]; Kazakov, Alexey E. ^[2]; Incha, Matthew R. ^[3]; Nava, Alberto A. ^[3];

^[3]; Valencia, Luis E. ^[3]; Keasling, Jay D. ^[4]; Rajeev, Lara ^[2];

^[3]

University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States); Danish Technical University, Lyngby (Denmark); Shenzhen Institutes for Advanced Technologies (China)

This report presents multi-genome evidence that REC protein family expansion occurs when the emergence of new pathways gives rise to functional discordance. Specificity between residues in REC domain containing response regulators with paired histidine kinases is under negative purifying selection, constrained by the presence of other bacterial two-component systems signaling cascades that share sequence and structural identity. Presuming that the two-component systems can evolve by neutral amino acid changes (neutral drift) when purifying evolutionary constraints are relaxed, how might the REC protein family expand by amino acid changes when these constraints remain intact? Using an unsupervised machine learning approach to observe the sequence landscape of REC domains across long phylogenetic distances, we find that within-gene recombination, a subcategory of gene conversion, switched the effector domain and, consequently, the regulatory context of a duplicated response regulator from transcriptional regulation by σ54 to that by σ70. We determined that the recombined response regulator diverged from its parent by episodic diversifying selection and neutral drift. Functional experiments of the parent of recombined response regulators in a model Pseudomonas putida KT2440 model system revealed that the parent and recombined response regulators sense and respond to different carboxylic acids. Finally, a residue-switching experiment using structural predictions and functional characterization suggests that the new residues in the recombined regulator could form a new interaction interface and mediate condition-specific phosphotransfer. Overall, our study finds that genetic perturbations can create conditions of functional discordance, whereby the REC protein family can evolve by episodic diversifying selection.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)

Grant/Contract Number:: 2018253421; AC02-05CH11231

OSTI ID:: 2221817

Journal Information:: mBio (Online), Vol. 14, Issue 6; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
large protein families
two-component regulatory systems
evolution
gene regulation
genetic recombination
domain swapping
signal transduction
response regulator

Title: REC protein family expansion by the emergence of a new signaling pathway

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