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Title: Loss of protein synthesis quality control in host-restricted organisms

Abstract

Intracellular organisms, such as obligate parasites and endosymbionts, typically possess small genomes due to continuous genome decay caused by an environment with alleviated natural selection. Previously, a few species with highly reduced genomes, including the intracellular pathogens Mycoplasma and Microsporidia , have been shown to carry degenerated editing domains in aminoacyl-tRNA synthetases. These defects in the protein synthesis machinery cause inaccurate translation of the genetic code, resulting in significant statistical errors in protein sequences that are thought to help parasites to escape immune response of a host. In this study we analyzed 10,423 complete bacterial genomes to assess conservation of the editing domains in tRNA synthetases, including LeuRS, IleRS, ValRS, ThrRS, AlaRS, and PheRS. We found that, while the editing domains remain intact in free-living species, they are degenerated in the overwhelming majority of host-restricted bacteria. Our work illustrates that massive genome erosion triggered by an intracellular lifestyle eradicates one of the most fundamental components of a living cell: the system responsible for proofreading of amino acid selection for protein synthesis. This finding suggests that inaccurate translation of the genetic code might be a general phenomenon among intercellular organisms with reduced genomes.

Authors:
; ; ; ; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1482775
Grant/Contract Number:  
FG02-98ER20311
Resource Type:
Journal Article: Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Melnikov, Sergey V., van den Elzen, Antonia, Stevens, David L., Thoreen, Carson C., and Söll, Dieter. Loss of protein synthesis quality control in host-restricted organisms. United States: N. p., 2018. Web. doi:10.1073/pnas.1815992115.
Melnikov, Sergey V., van den Elzen, Antonia, Stevens, David L., Thoreen, Carson C., & Söll, Dieter. Loss of protein synthesis quality control in host-restricted organisms. United States. doi:10.1073/pnas.1815992115.
Melnikov, Sergey V., van den Elzen, Antonia, Stevens, David L., Thoreen, Carson C., and Söll, Dieter. Mon . "Loss of protein synthesis quality control in host-restricted organisms". United States. doi:10.1073/pnas.1815992115.
@article{osti_1482775,
title = {Loss of protein synthesis quality control in host-restricted organisms},
author = {Melnikov, Sergey V. and van den Elzen, Antonia and Stevens, David L. and Thoreen, Carson C. and Söll, Dieter},
abstractNote = {Intracellular organisms, such as obligate parasites and endosymbionts, typically possess small genomes due to continuous genome decay caused by an environment with alleviated natural selection. Previously, a few species with highly reduced genomes, including the intracellular pathogens Mycoplasma and Microsporidia , have been shown to carry degenerated editing domains in aminoacyl-tRNA synthetases. These defects in the protein synthesis machinery cause inaccurate translation of the genetic code, resulting in significant statistical errors in protein sequences that are thought to help parasites to escape immune response of a host. In this study we analyzed 10,423 complete bacterial genomes to assess conservation of the editing domains in tRNA synthetases, including LeuRS, IleRS, ValRS, ThrRS, AlaRS, and PheRS. We found that, while the editing domains remain intact in free-living species, they are degenerated in the overwhelming majority of host-restricted bacteria. Our work illustrates that massive genome erosion triggered by an intracellular lifestyle eradicates one of the most fundamental components of a living cell: the system responsible for proofreading of amino acid selection for protein synthesis. This finding suggests that inaccurate translation of the genetic code might be a general phenomenon among intercellular organisms with reduced genomes.},
doi = {10.1073/pnas.1815992115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = ,
volume = ,
place = {United States},
year = {Mon Nov 19 00:00:00 EST 2018},
month = {Mon Nov 19 00:00:00 EST 2018}
}

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