Antisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria

ABSTRACT Noncoding RNAs, including antisense RNAs (asRNAs) that originate from the complementary strand of protein-coding genes, are involved in the regulation of gene expression in all domains of life. Recent application of deep-sequencing technologies has revealed that the transcription of asRNAs...

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Autores principales:	Rahul Raghavan, Daniel B. Sloan, Howard Ochman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/beb8e1823cb54349b28a05137b507885
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spelling	oai:doaj.org-article:beb8e1823cb54349b28a05137b5078852021-11-15T15:39:09ZAntisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria10.1128/mBio.00156-122150-7511https://doaj.org/article/beb8e1823cb54349b28a05137b5078852012-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00156-12https://doaj.org/toc/2150-7511ABSTRACT Noncoding RNAs, including antisense RNAs (asRNAs) that originate from the complementary strand of protein-coding genes, are involved in the regulation of gene expression in all domains of life. Recent application of deep-sequencing technologies has revealed that the transcription of asRNAs occurs genome-wide in bacteria. Although the role of the vast majority of asRNAs remains unknown, it is often assumed that their presence implies important regulatory functions, similar to those of other noncoding RNAs. Alternatively, many antisense transcripts may be produced by chance transcription events from promoter-like sequences that result from the degenerate nature of bacterial transcription factor binding sites. To investigate the biological relevance of antisense transcripts, we compared genome-wide patterns of asRNA expression in closely related enteric bacteria, Escherichia coli and Salmonella enterica serovar Typhimurium, by performing strand-specific transcriptome sequencing. Although antisense transcripts are abundant in both species, less than 3% of asRNAs are expressed at high levels in both species, and only about 14% appear to be conserved among species. And unlike the promoters of protein-coding genes, asRNA promoters show no evidence of sequence conservation between, or even within, species. Our findings suggest that many or even most bacterial asRNAs are nonadaptive by-products of the cell’s transcription machinery. IMPORTANCE Application of high-throughput methods has revealed the expression throughout bacterial genomes of transcripts encoded on the strand complementary to protein-coding genes. Because transcription is costly, it is usually assumed that these transcripts, termed antisense RNAs (asRNAs), serve some function; however, the role of most asRNAs is unclear, raising questions about their relevance in cellular processes. Because natural selection conserves functional elements, comparisons between related species provide a method for assessing functionality genome-wide. Applying such an approach, we assayed all transcripts in two closely related bacteria, Escherichia coli and Salmonella enterica serovar Typhimurium, and demonstrate that, although the levels of genome-wide antisense transcription are similarly high in both bacteria, only a small fraction of asRNAs are shared across species. Moreover, the promoters associated with asRNAs show no evidence of sequence conservation between, or even within, species. These findings indicate that despite the genome-wide transcription of asRNAs, many of these transcripts are likely nonfunctional.Rahul RaghavanDaniel B. SloanHoward OchmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 4 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Rahul Raghavan Daniel B. Sloan Howard Ochman Antisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria
description	ABSTRACT Noncoding RNAs, including antisense RNAs (asRNAs) that originate from the complementary strand of protein-coding genes, are involved in the regulation of gene expression in all domains of life. Recent application of deep-sequencing technologies has revealed that the transcription of asRNAs occurs genome-wide in bacteria. Although the role of the vast majority of asRNAs remains unknown, it is often assumed that their presence implies important regulatory functions, similar to those of other noncoding RNAs. Alternatively, many antisense transcripts may be produced by chance transcription events from promoter-like sequences that result from the degenerate nature of bacterial transcription factor binding sites. To investigate the biological relevance of antisense transcripts, we compared genome-wide patterns of asRNA expression in closely related enteric bacteria, Escherichia coli and Salmonella enterica serovar Typhimurium, by performing strand-specific transcriptome sequencing. Although antisense transcripts are abundant in both species, less than 3% of asRNAs are expressed at high levels in both species, and only about 14% appear to be conserved among species. And unlike the promoters of protein-coding genes, asRNA promoters show no evidence of sequence conservation between, or even within, species. Our findings suggest that many or even most bacterial asRNAs are nonadaptive by-products of the cell’s transcription machinery. IMPORTANCE Application of high-throughput methods has revealed the expression throughout bacterial genomes of transcripts encoded on the strand complementary to protein-coding genes. Because transcription is costly, it is usually assumed that these transcripts, termed antisense RNAs (asRNAs), serve some function; however, the role of most asRNAs is unclear, raising questions about their relevance in cellular processes. Because natural selection conserves functional elements, comparisons between related species provide a method for assessing functionality genome-wide. Applying such an approach, we assayed all transcripts in two closely related bacteria, Escherichia coli and Salmonella enterica serovar Typhimurium, and demonstrate that, although the levels of genome-wide antisense transcription are similarly high in both bacteria, only a small fraction of asRNAs are shared across species. Moreover, the promoters associated with asRNAs show no evidence of sequence conservation between, or even within, species. These findings indicate that despite the genome-wide transcription of asRNAs, many of these transcripts are likely nonfunctional.
format	article
author	Rahul Raghavan Daniel B. Sloan Howard Ochman
author_facet	Rahul Raghavan Daniel B. Sloan Howard Ochman
author_sort	Rahul Raghavan
title	Antisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria
title_short	Antisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria
title_full	Antisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria
title_fullStr	Antisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria
title_full_unstemmed	Antisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria
title_sort	antisense transcription is pervasive but rarely conserved in enteric bacteria
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/beb8e1823cb54349b28a05137b507885
work_keys_str_mv	AT rahulraghavan antisensetranscriptionispervasivebutrarelyconservedinentericbacteria AT danielbsloan antisensetranscriptionispervasivebutrarelyconservedinentericbacteria AT howardochman antisensetranscriptionispervasivebutrarelyconservedinentericbacteria
_version_	1718427792568221696

Antisense Transcription Is Pervasive but Rarely Conserved in Enteric Bacteria

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