How Bacterial Chemoreceptors Evolve Novel Ligand Specificities

ABSTRACT Chemoreceptor-based signaling pathways are among the major modes of bacterial signal transduction, and Pseudomonas aeruginosa PAO1 is an important model to study their function. Of the 26 chemoreceptors of this strain, PctA has a broad ligand range and responds to most of the proteinogenic...

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Autores principales:	José Antonio Gavira, Vadim M. Gumerov, Miriam Rico-Jiménez, Marharyta Petukh, Amit A. Upadhyay, Alvaro Ortega, Miguel A. Matilla, Igor B. Zhulin, Tino Krell
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	cache domains chemotaxis evolution ligands signal transduction Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/137df719cfa54b34b83335f426bb5523
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spelling	oai:doaj.org-article:137df719cfa54b34b83335f426bb55232021-11-15T15:56:58ZHow Bacterial Chemoreceptors Evolve Novel Ligand Specificities10.1128/mBio.03066-192150-7511https://doaj.org/article/137df719cfa54b34b83335f426bb55232020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03066-19https://doaj.org/toc/2150-7511ABSTRACT Chemoreceptor-based signaling pathways are among the major modes of bacterial signal transduction, and Pseudomonas aeruginosa PAO1 is an important model to study their function. Of the 26 chemoreceptors of this strain, PctA has a broad ligand range and responds to most of the proteinogenic amino acids, whereas PctB and PctC have a much narrower range and show strong ligand preference for l-glutamine and γ-aminobutyrate, respectively. Using several comparative genomics approaches, we show that these receptors are paralogs: pctA gene duplication in the common ancestor of the genus Pseudomonas led to pctC, whereas pctB originated through another, independent pctA duplication in the common ancestor of P. aeruginosa. Thus, the broad-range amino acid chemoreceptor was evolutionarily older, and chemoreceptors that complemented “missing” amino acid sensing abilities arose later in specific Pseudomonas lineages. Using comparative sequence analysis, newly solved crystal structures of PctA, PctB, and PctC ligand-binding domains, and their molecular dynamics simulations, we identified a conserved amino acid recognition motif and changes in the ligand-binding pocket that led to novel ligand specificities. In addition, we determined major forces driving the evolution of this group of chemoreceptors. IMPORTANCE Many bacteria possess a large number of chemoreceptors that recognize a variety of different compounds. More than 60% of the genomes analyzed in this study contain paralogous chemoreceptors, suggesting that they emerge with high frequency. We provide first insight on how paralogous receptors have evolved and show that two chemoreceptors with a narrow ligand range have evolved from an ancestral protein with a broad chemoeffector spectrum. Protein structures show that multiple changes in the ligand-binding site account for the differences in the ligand spectrum. This work lays the ground for further studies aimed at establishing whether the principles of ligand-binding evolution reported here can be generalized for a wider spectrum of sensory proteins in bacteria.José Antonio GaviraVadim M. GumerovMiriam Rico-JiménezMarharyta PetukhAmit A. UpadhyayAlvaro OrtegaMiguel A. MatillaIgor B. ZhulinTino KrellAmerican Society for Microbiologyarticlecache domainschemotaxisevolutionligandssignal transductionMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	cache domains chemotaxis evolution ligands signal transduction Microbiology QR1-502
spellingShingle	cache domains chemotaxis evolution ligands signal transduction Microbiology QR1-502 José Antonio Gavira Vadim M. Gumerov Miriam Rico-Jiménez Marharyta Petukh Amit A. Upadhyay Alvaro Ortega Miguel A. Matilla Igor B. Zhulin Tino Krell How Bacterial Chemoreceptors Evolve Novel Ligand Specificities
description	ABSTRACT Chemoreceptor-based signaling pathways are among the major modes of bacterial signal transduction, and Pseudomonas aeruginosa PAO1 is an important model to study their function. Of the 26 chemoreceptors of this strain, PctA has a broad ligand range and responds to most of the proteinogenic amino acids, whereas PctB and PctC have a much narrower range and show strong ligand preference for l-glutamine and γ-aminobutyrate, respectively. Using several comparative genomics approaches, we show that these receptors are paralogs: pctA gene duplication in the common ancestor of the genus Pseudomonas led to pctC, whereas pctB originated through another, independent pctA duplication in the common ancestor of P. aeruginosa. Thus, the broad-range amino acid chemoreceptor was evolutionarily older, and chemoreceptors that complemented “missing” amino acid sensing abilities arose later in specific Pseudomonas lineages. Using comparative sequence analysis, newly solved crystal structures of PctA, PctB, and PctC ligand-binding domains, and their molecular dynamics simulations, we identified a conserved amino acid recognition motif and changes in the ligand-binding pocket that led to novel ligand specificities. In addition, we determined major forces driving the evolution of this group of chemoreceptors. IMPORTANCE Many bacteria possess a large number of chemoreceptors that recognize a variety of different compounds. More than 60% of the genomes analyzed in this study contain paralogous chemoreceptors, suggesting that they emerge with high frequency. We provide first insight on how paralogous receptors have evolved and show that two chemoreceptors with a narrow ligand range have evolved from an ancestral protein with a broad chemoeffector spectrum. Protein structures show that multiple changes in the ligand-binding site account for the differences in the ligand spectrum. This work lays the ground for further studies aimed at establishing whether the principles of ligand-binding evolution reported here can be generalized for a wider spectrum of sensory proteins in bacteria.
format	article
author	José Antonio Gavira Vadim M. Gumerov Miriam Rico-Jiménez Marharyta Petukh Amit A. Upadhyay Alvaro Ortega Miguel A. Matilla Igor B. Zhulin Tino Krell
author_facet	José Antonio Gavira Vadim M. Gumerov Miriam Rico-Jiménez Marharyta Petukh Amit A. Upadhyay Alvaro Ortega Miguel A. Matilla Igor B. Zhulin Tino Krell
author_sort	José Antonio Gavira
title	How Bacterial Chemoreceptors Evolve Novel Ligand Specificities
title_short	How Bacterial Chemoreceptors Evolve Novel Ligand Specificities
title_full	How Bacterial Chemoreceptors Evolve Novel Ligand Specificities
title_fullStr	How Bacterial Chemoreceptors Evolve Novel Ligand Specificities
title_full_unstemmed	How Bacterial Chemoreceptors Evolve Novel Ligand Specificities
title_sort	how bacterial chemoreceptors evolve novel ligand specificities
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/137df719cfa54b34b83335f426bb5523
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_version_	1718427071772884992

How Bacterial Chemoreceptors Evolve Novel Ligand Specificities

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