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Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus

SIMPLE SUMMARY: Bacteria belonging to the Ralstonia genus are of great interest for study since this genus includes both phytopathogenic species and soil opportunistic human pathogens, forming two phylogenetic branches. The difference in phenotype of related species is formed by differences in how p...

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Autores principales: Korenskaia, Aleksandra Y., Matushkin, Yury G., Mustafin, Zakhar S., Lashin, Sergey A., Klimenko, Alexandra I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10604486/
https://www.ncbi.nlm.nih.gov/pubmed/37887048
http://dx.doi.org/10.3390/biology12101338
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author Korenskaia, Aleksandra Y.
Matushkin, Yury G.
Mustafin, Zakhar S.
Lashin, Sergey A.
Klimenko, Alexandra I.
author_facet Korenskaia, Aleksandra Y.
Matushkin, Yury G.
Mustafin, Zakhar S.
Lashin, Sergey A.
Klimenko, Alexandra I.
author_sort Korenskaia, Aleksandra Y.
collection PubMed
description SIMPLE SUMMARY: Bacteria belonging to the Ralstonia genus are of great interest for study since this genus includes both phytopathogenic species and soil opportunistic human pathogens, forming two phylogenetic branches. The difference in phenotype of related species is formed by differences in how proteins and other molecules bacteria synthesize, as well as the level of their synthesis. In this study, we investigate the evolution of the Ralstonia genus, focusing on characteristics of a particular stage of protein synthesis. This is a stage at which the protein sequence is synthesized, named translation elongation. The efficiency of this stage plays a role in the modulating of gene expression, while characteristics of this stage considered being more conservative allow us to use it for comparison at the genus level. We calculated the elongation efficiency based on genomic data and found that characteristics of translation elongation efficiency optimization diverge in accordance with the phylogeny of Ralstonia. Differences in these characteristics of genomes as a whole are also reflected in differences in the efficiency of translation elongation of individual genes, resulting in differences in sets of potentially highly expressed genes in soil and phytopathogenic bacteria. These results are valuable for understanding the evolution and adaptation of bacteria in different environments. ABSTRACT: Translation efficiency modulates gene expression in prokaryotes. The comparative analysis of translation elongation efficiency characteristics of Ralstonia genus bacteria genomes revealed that these characteristics diverge in accordance with the phylogeny of Ralstonia. The first branch of this genus is a group of bacteria commonly found in moist environments such as soil and water that includes the species R. mannitolilytica, R. insidiosa, and R. pickettii, which are also described as nosocomial infection pathogens. In contrast, the second branch is plant pathogenic bacteria consisting of R. solanacearum, R. pseudosolanacearum, and R. syzygii. We found that the soil Ralstonia have a significantly lower number and energy of potential secondary structures in mRNA and an increased role of codon usage bias in the optimization of highly expressed genes’ translation elongation efficiency, not only compared to phytopathogenic Ralstonia but also to Cupriavidus necator, which is closely related to the Ralstonia genus. The observed alterations in translation elongation efficiency of orthologous genes are also reflected in the difference of potentially highly expressed gene’ sets’ content among Ralstonia branches with different lifestyles. Analysis of translation elongation efficiency characteristics can be considered a promising approach for studying complex mechanisms that determine the evolution and adaptation of bacteria in various environments.
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spelling pubmed-106044862023-10-28 Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus Korenskaia, Aleksandra Y. Matushkin, Yury G. Mustafin, Zakhar S. Lashin, Sergey A. Klimenko, Alexandra I. Biology (Basel) Article SIMPLE SUMMARY: Bacteria belonging to the Ralstonia genus are of great interest for study since this genus includes both phytopathogenic species and soil opportunistic human pathogens, forming two phylogenetic branches. The difference in phenotype of related species is formed by differences in how proteins and other molecules bacteria synthesize, as well as the level of their synthesis. In this study, we investigate the evolution of the Ralstonia genus, focusing on characteristics of a particular stage of protein synthesis. This is a stage at which the protein sequence is synthesized, named translation elongation. The efficiency of this stage plays a role in the modulating of gene expression, while characteristics of this stage considered being more conservative allow us to use it for comparison at the genus level. We calculated the elongation efficiency based on genomic data and found that characteristics of translation elongation efficiency optimization diverge in accordance with the phylogeny of Ralstonia. Differences in these characteristics of genomes as a whole are also reflected in differences in the efficiency of translation elongation of individual genes, resulting in differences in sets of potentially highly expressed genes in soil and phytopathogenic bacteria. These results are valuable for understanding the evolution and adaptation of bacteria in different environments. ABSTRACT: Translation efficiency modulates gene expression in prokaryotes. The comparative analysis of translation elongation efficiency characteristics of Ralstonia genus bacteria genomes revealed that these characteristics diverge in accordance with the phylogeny of Ralstonia. The first branch of this genus is a group of bacteria commonly found in moist environments such as soil and water that includes the species R. mannitolilytica, R. insidiosa, and R. pickettii, which are also described as nosocomial infection pathogens. In contrast, the second branch is plant pathogenic bacteria consisting of R. solanacearum, R. pseudosolanacearum, and R. syzygii. We found that the soil Ralstonia have a significantly lower number and energy of potential secondary structures in mRNA and an increased role of codon usage bias in the optimization of highly expressed genes’ translation elongation efficiency, not only compared to phytopathogenic Ralstonia but also to Cupriavidus necator, which is closely related to the Ralstonia genus. The observed alterations in translation elongation efficiency of orthologous genes are also reflected in the difference of potentially highly expressed gene’ sets’ content among Ralstonia branches with different lifestyles. Analysis of translation elongation efficiency characteristics can be considered a promising approach for studying complex mechanisms that determine the evolution and adaptation of bacteria in various environments. MDPI 2023-10-16 /pmc/articles/PMC10604486/ /pubmed/37887048 http://dx.doi.org/10.3390/biology12101338 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Korenskaia, Aleksandra Y.
Matushkin, Yury G.
Mustafin, Zakhar S.
Lashin, Sergey A.
Klimenko, Alexandra I.
Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus
title Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus
title_full Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus
title_fullStr Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus
title_full_unstemmed Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus
title_short Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus
title_sort bioinformatic analysis reveals the role of translation elongation efficiency optimisation in the evolution of ralstonia genus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10604486/
https://www.ncbi.nlm.nih.gov/pubmed/37887048
http://dx.doi.org/10.3390/biology12101338
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