Burning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?

ABSTRACT Regulatory RNAs have emerged as ubiquitous gene regulators in all bacterial species studied to date. The combination of sequence-specific RNA interactions and malleable RNA structure has allowed regulatory RNA to adopt different mechanisms of gene regulation in a diversity of genetic backgr...

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Autores principales:	Daniel G. Mediati, David Lalaouna, Jai J. Tree
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	3′ UTR Hfq RNA decay RNase J evolution small RNA Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3f39776b40374676984e58606645f9fc
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spelling	oai:doaj.org-article:3f39776b40374676984e58606645f9fc2021-11-10T18:37:50ZBurning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?10.1128/mBio.01041-212150-7511https://doaj.org/article/3f39776b40374676984e58606645f9fc2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01041-21https://doaj.org/toc/2150-7511ABSTRACT Regulatory RNAs have emerged as ubiquitous gene regulators in all bacterial species studied to date. The combination of sequence-specific RNA interactions and malleable RNA structure has allowed regulatory RNA to adopt different mechanisms of gene regulation in a diversity of genetic backgrounds. In the model Gammaproteobacteria Escherichia coli and Salmonella, the regulatory RNA chaperone Hfq appears to play a global role in gene regulation, directly controlling ∼20 to 25% of the entire transcriptome. While the model Firmicutes Bacillus subtilis and Staphylococcus aureus encode a Hfq homologue, its role has been significantly depreciated. These bacteria also have marked differences in RNA turnover. E. coli and Salmonella degrade RNA through internal endonucleolytic and 3′→5′ exonucleolytic cleavage that appears to allow transient accumulation of mRNA 3′ UTR cleavage fragments that contain stabilizing 3′ structures. In contrast, B. subtilis and S. aureus are able to exonucleolytically attack internally cleaved RNA from both the 5′ and 3′ ends, efficiently degrading mRNA 3′ UTR fragments. Here, we propose that the lack of 5′→3′ exoribonuclease activity in Gammaproteobacteria has allowed the accumulation of mRNA 3′ UTR ends as the “default” setting. This in turn may have provided a larger pool of unconstrained RNA sequences that has fueled the expansion of Hfq function and small RNA (sRNA) regulation in E. coli and Salmonella. Conversely, the exoribonuclease RNase J may be a significant barrier to the evolution of 3′ UTR sRNAs in B. subtilis and S. aureus that has limited the pool of RNA ligands available to Hfq and other sRNA chaperones, depreciating their function in these model Firmicutes.Daniel G. MediatiDavid LalaounaJai J. TreeAmerican Society for Microbiologyarticle3′ UTRHfqRNA decayRNase Jevolutionsmall RNAMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	3′ UTR Hfq RNA decay RNase J evolution small RNA Microbiology QR1-502
spellingShingle	3′ UTR Hfq RNA decay RNase J evolution small RNA Microbiology QR1-502 Daniel G. Mediati David Lalaouna Jai J. Tree Burning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?
description	ABSTRACT Regulatory RNAs have emerged as ubiquitous gene regulators in all bacterial species studied to date. The combination of sequence-specific RNA interactions and malleable RNA structure has allowed regulatory RNA to adopt different mechanisms of gene regulation in a diversity of genetic backgrounds. In the model Gammaproteobacteria Escherichia coli and Salmonella, the regulatory RNA chaperone Hfq appears to play a global role in gene regulation, directly controlling ∼20 to 25% of the entire transcriptome. While the model Firmicutes Bacillus subtilis and Staphylococcus aureus encode a Hfq homologue, its role has been significantly depreciated. These bacteria also have marked differences in RNA turnover. E. coli and Salmonella degrade RNA through internal endonucleolytic and 3′→5′ exonucleolytic cleavage that appears to allow transient accumulation of mRNA 3′ UTR cleavage fragments that contain stabilizing 3′ structures. In contrast, B. subtilis and S. aureus are able to exonucleolytically attack internally cleaved RNA from both the 5′ and 3′ ends, efficiently degrading mRNA 3′ UTR fragments. Here, we propose that the lack of 5′→3′ exoribonuclease activity in Gammaproteobacteria has allowed the accumulation of mRNA 3′ UTR ends as the “default” setting. This in turn may have provided a larger pool of unconstrained RNA sequences that has fueled the expansion of Hfq function and small RNA (sRNA) regulation in E. coli and Salmonella. Conversely, the exoribonuclease RNase J may be a significant barrier to the evolution of 3′ UTR sRNAs in B. subtilis and S. aureus that has limited the pool of RNA ligands available to Hfq and other sRNA chaperones, depreciating their function in these model Firmicutes.
format	article
author	Daniel G. Mediati David Lalaouna Jai J. Tree
author_facet	Daniel G. Mediati David Lalaouna Jai J. Tree
author_sort	Daniel G. Mediati
title	Burning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?
title_short	Burning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?
title_full	Burning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?
title_fullStr	Burning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?
title_full_unstemmed	Burning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?
title_sort	burning the candle at both ends: have exoribonucleases driven divergence of regulatory rna mechanisms in bacteria?
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/3f39776b40374676984e58606645f9fc
work_keys_str_mv	AT danielgmediati burningthecandleatbothendshaveexoribonucleasesdrivendivergenceofregulatoryrnamechanismsinbacteria AT davidlalaouna burningthecandleatbothendshaveexoribonucleasesdrivendivergenceofregulatoryrnamechanismsinbacteria AT jaijtree burningthecandleatbothendshaveexoribonucleasesdrivendivergenceofregulatoryrnamechanismsinbacteria
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Burning the Candle at Both Ends: Have Exoribonucleases Driven Divergence of Regulatory RNA Mechanisms in Bacteria?

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