Release of Nonstop Ribosomes Is Essential

ABSTRACT Bacterial ribosomes frequently translate to the 3′ end of an mRNA without terminating at a stop codon. Almost all bacteria use the transfer-messenger RNA (tmRNA)-based trans-translation pathway to release these “nonstop” ribosomes and maintain protein synthesis capacity. trans-translation i...

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Autores principales: Heather A. Feaga, Patrick H. Viollier, Kenneth C. Keiler
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:fe1580f287ca4df3820ac24585f705902021-11-15T15:47:03ZRelease of Nonstop Ribosomes Is Essential10.1128/mBio.01916-142150-7511https://doaj.org/article/fe1580f287ca4df3820ac24585f705902014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01916-14https://doaj.org/toc/2150-7511ABSTRACT Bacterial ribosomes frequently translate to the 3′ end of an mRNA without terminating at a stop codon. Almost all bacteria use the transfer-messenger RNA (tmRNA)-based trans-translation pathway to release these “nonstop” ribosomes and maintain protein synthesis capacity. trans-translation is essential in some species, but in others, such as Caulobacter crescentus, trans-translation can be inactivated. To determine why trans-translation is dispensable in C. crescentus, a Tn-seq screen was used to identify genes that specifically alter growth in cells lacking ssrA, the gene encoding tmRNA. One of these genes, CC1214, was essential in ΔssrA cells. Purified CC1214 protein could release nonstop ribosomes in vitro. CC1214 is a homolog of the Escherichia coli ArfB protein, and using the CC1214 sequence, ArfB homologs were identified in the majority of bacterial phyla. Most species in which ssrA has been deleted contain an ArfB homolog, suggesting that release of nonstop ribosomes may be essential in most or all bacteria. IMPORTANCE Genes that are conserved across large phylogenetic distances are expected to confer a selective advantage. The genes required for trans-translation, ssrA and smpB, have been found in >99% of sequenced bacterial genomes, suggesting that they are broadly important. However, these genes can be deleted in some species without loss of viability. The identification and characterization of C. crescentus ArfB reveals why trans-translation is not essential in C. crescentus and suggests that many other bacteria are likely to use ArfB to survive when trans-translation is compromised.Heather A. FeagaPatrick H. ViollierKenneth C. KeilerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Heather A. Feaga
Patrick H. Viollier
Kenneth C. Keiler
Release of Nonstop Ribosomes Is Essential
description ABSTRACT Bacterial ribosomes frequently translate to the 3′ end of an mRNA without terminating at a stop codon. Almost all bacteria use the transfer-messenger RNA (tmRNA)-based trans-translation pathway to release these “nonstop” ribosomes and maintain protein synthesis capacity. trans-translation is essential in some species, but in others, such as Caulobacter crescentus, trans-translation can be inactivated. To determine why trans-translation is dispensable in C. crescentus, a Tn-seq screen was used to identify genes that specifically alter growth in cells lacking ssrA, the gene encoding tmRNA. One of these genes, CC1214, was essential in ΔssrA cells. Purified CC1214 protein could release nonstop ribosomes in vitro. CC1214 is a homolog of the Escherichia coli ArfB protein, and using the CC1214 sequence, ArfB homologs were identified in the majority of bacterial phyla. Most species in which ssrA has been deleted contain an ArfB homolog, suggesting that release of nonstop ribosomes may be essential in most or all bacteria. IMPORTANCE Genes that are conserved across large phylogenetic distances are expected to confer a selective advantage. The genes required for trans-translation, ssrA and smpB, have been found in >99% of sequenced bacterial genomes, suggesting that they are broadly important. However, these genes can be deleted in some species without loss of viability. The identification and characterization of C. crescentus ArfB reveals why trans-translation is not essential in C. crescentus and suggests that many other bacteria are likely to use ArfB to survive when trans-translation is compromised.
format article
author Heather A. Feaga
Patrick H. Viollier
Kenneth C. Keiler
author_facet Heather A. Feaga
Patrick H. Viollier
Kenneth C. Keiler
author_sort Heather A. Feaga
title Release of Nonstop Ribosomes Is Essential
title_short Release of Nonstop Ribosomes Is Essential
title_full Release of Nonstop Ribosomes Is Essential
title_fullStr Release of Nonstop Ribosomes Is Essential
title_full_unstemmed Release of Nonstop Ribosomes Is Essential
title_sort release of nonstop ribosomes is essential
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/fe1580f287ca4df3820ac24585f70590
work_keys_str_mv AT heatherafeaga releaseofnonstopribosomesisessential
AT patrickhviollier releaseofnonstopribosomesisessential
AT kennethckeiler releaseofnonstopribosomesisessential
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