Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>

ABSTRACT When prokaryotic cells acquire mutations, encounter translation-inhibiting substances, or experience adverse environmental conditions that limit their ability to synthesize proteins, transcription can become uncoupled from translation. Such uncoupling is known to suppress transcription of p...

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Autores principales:	Eric G. Matson, Adam Z. Rosenthal, Xinning Zhang, Jared R. Leadbetter
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5eed56bb76fd4c2f8363fd8b2a1952dc
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spelling	oai:doaj.org-article:5eed56bb76fd4c2f8363fd8b2a1952dc2021-11-15T15:42:31ZGenome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>10.1128/mBio.00869-132150-7511https://doaj.org/article/5eed56bb76fd4c2f8363fd8b2a1952dc2013-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00869-13https://doaj.org/toc/2150-7511ABSTRACT When prokaryotic cells acquire mutations, encounter translation-inhibiting substances, or experience adverse environmental conditions that limit their ability to synthesize proteins, transcription can become uncoupled from translation. Such uncoupling is known to suppress transcription of protein-encoding genes in bacteria. Here we show that the trace element selenium controls transcription of the gene for the selenocysteine-utilizing enzyme formate dehydrogenase (fdhFSec) through a translation-coupled mechanism in the termite gut symbiont Treponema primitia, a member of the bacterial phylum Spirochaetes. We also evaluated changes in genome-wide transcriptional patterns caused by selenium limitation and by generally uncoupling translation from transcription via antibiotic-mediated inhibition of protein synthesis. We observed that inhibiting protein synthesis in T. primitia influences transcriptional patterns in unexpected ways. In addition to suppressing transcription of certain genes, the expected consequence of inhibiting protein synthesis, we found numerous examples in which transcription of genes and operons is truncated far downstream from putative promoters, is unchanged, or is even stimulated overall. These results indicate that gene regulation in bacteria allows for specific post-initiation transcriptional responses during periods of limited protein synthesis, which may depend both on translational coupling and on unclassified intrinsic elements of protein-encoding genes. IMPORTANCE A large body of literature demonstrates that the coupling of transcription and translation is a general and essential method by which bacteria regulate gene expression levels. However, the potential role of noncanonical amino acids in regulating transcriptional output via translational control remains, for the most part, undefined. Furthermore, the genome-wide transcriptional state in response to translational decoupling is not well quantified. The results presented here suggest that the noncanonical amino acid selenocysteine is able to tune transcription of an important metabolic gene via translational coupling. Furthermore, a genome-wide analysis reveals that transcriptional decoupling produces a wide-ranging effect and that this effect is not uniform. These results exemplify how growth conditions that impact translational processivity can rapidly feed back on transcriptional productivity of prespecified groups of genes, providing bacteria with an efficient response to environmental changes.Eric G. MatsonAdam Z. RosenthalXinning ZhangJared R. LeadbetterAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 6 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Eric G. Matson Adam Z. Rosenthal Xinning Zhang Jared R. Leadbetter Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>
description	ABSTRACT When prokaryotic cells acquire mutations, encounter translation-inhibiting substances, or experience adverse environmental conditions that limit their ability to synthesize proteins, transcription can become uncoupled from translation. Such uncoupling is known to suppress transcription of protein-encoding genes in bacteria. Here we show that the trace element selenium controls transcription of the gene for the selenocysteine-utilizing enzyme formate dehydrogenase (fdhFSec) through a translation-coupled mechanism in the termite gut symbiont Treponema primitia, a member of the bacterial phylum Spirochaetes. We also evaluated changes in genome-wide transcriptional patterns caused by selenium limitation and by generally uncoupling translation from transcription via antibiotic-mediated inhibition of protein synthesis. We observed that inhibiting protein synthesis in T. primitia influences transcriptional patterns in unexpected ways. In addition to suppressing transcription of certain genes, the expected consequence of inhibiting protein synthesis, we found numerous examples in which transcription of genes and operons is truncated far downstream from putative promoters, is unchanged, or is even stimulated overall. These results indicate that gene regulation in bacteria allows for specific post-initiation transcriptional responses during periods of limited protein synthesis, which may depend both on translational coupling and on unclassified intrinsic elements of protein-encoding genes. IMPORTANCE A large body of literature demonstrates that the coupling of transcription and translation is a general and essential method by which bacteria regulate gene expression levels. However, the potential role of noncanonical amino acids in regulating transcriptional output via translational control remains, for the most part, undefined. Furthermore, the genome-wide transcriptional state in response to translational decoupling is not well quantified. The results presented here suggest that the noncanonical amino acid selenocysteine is able to tune transcription of an important metabolic gene via translational coupling. Furthermore, a genome-wide analysis reveals that transcriptional decoupling produces a wide-ranging effect and that this effect is not uniform. These results exemplify how growth conditions that impact translational processivity can rapidly feed back on transcriptional productivity of prespecified groups of genes, providing bacteria with an efficient response to environmental changes.
format	article
author	Eric G. Matson Adam Z. Rosenthal Xinning Zhang Jared R. Leadbetter
author_facet	Eric G. Matson Adam Z. Rosenthal Xinning Zhang Jared R. Leadbetter
author_sort	Eric G. Matson
title	Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>
title_short	Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>
title_full	Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>
title_fullStr	Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>
title_full_unstemmed	Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>
title_sort	genome-wide effects of selenium and translational uncoupling on transcription in the termite gut symbiont <named-content content-type="genus-species">treponema primitia</named-content>
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/5eed56bb76fd4c2f8363fd8b2a1952dc
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Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont <named-content content-type="genus-species">Treponema primitia</named-content>

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