title: Evolution of bacterial protein-tyrosine kinases and their relaxed specificity toward substrates.
abstract: It has often been speculated that bacterial protein-tyrosine kinases (BY-kinases) evolve rapidly and maintain relaxed substrate specificity to quickly adopt new substrates when evolutionary pressure in that direction arises. Here, we report a phylogenomic and biochemical analysis of BY-kinases, and their relationship to substrates aimed to validate this hypothesis. Our results suggest that BY-kinases are ubiquitously distributed in bacterial phyla and underwent a complex evolutionary history, affected considerably by gene duplications and horizontal gene transfer events. This is consistent with the fact that the BY-kinase sequences represent a high level of substitution saturation and have a higher evolutionary rate compared with other bacterial genes. On the basis of similarity networks, we could classify BY kinases into three main groups with 14 subgroups. Extensive sequence conservation was observed only around the three canonical Walker motifs, whereas unique signatures proposed the functional speciation and diversification within some subgroups. The relationship between BY-kinases and their substrates was analyzed using a ubiquitous substrate (Ugd) and some Firmicute-specific substrates (YvyG and YjoA) from Bacillus subtilis. No evidence of coevolution between kinases and substrates at the sequence level was found. Seven BY-kinases, including well-characterized and previously uncharacterized ones, were used for experimental studies. Most of the tested kinases were able to phosphorylate substrates from B. subtilis (Ugd, YvyG, and YjoA), despite originating from very distant bacteria. Our results are consistent with the hypothesis that BY-kinases have evolved relaxed substrate specificity and are probably maintained as rapidly evolving platforms for adopting new substrates.
authors.affiliation: INRA-AgroParisTech UMR 1319, Micalis-CBAI, Thiverval-Grignon, France.
authors.forename: Lei
authors.initials: L
authors.lastname: Shi
authors.forename: Boyang
authors.initials: B
authors.lastname: Ji
authors.forename: Lorena
authors.initials: L
authors.lastname: Kolar-Znika
authors.forename: Ana
authors.initials: A
authors.lastname: Boskovic
authors.forename: Fanny
authors.initials: F
authors.lastname: Jadeau
authors.forename: Christophe
authors.initials: C
authors.lastname: Combet
authors.forename: Christophe
authors.initials: C
authors.lastname: Grangeasse
authors.forename: Damjan
authors.initials: D
authors.lastname: Franjevic
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Talla
authors.forename: Ivan
authors.initials: I
authors.lastname: Mijakovic
mesh_terms: D001412:Bacillus subtilis / Q000201:enzymology / Q000235:genetics*; D001426:Bacterial Proteins / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D011505:Protein-Tyrosine Kinases / Q000235:genetics* / Q000378:metabolism; D013379:Substrate Specificity / Q000502:physiology
chemical_list: D001426:Bacterial Proteins; D011505:Protein-Tyrosine Kinases
keywords: BY-kinases; bacterial protein kinases; kinase classification; kinase evolution; kinase-substrate coevolution; phylogeny
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