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Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont Treponema primitia

Matson, Eric G. and Rosenthal, Adam Z. and Zhang, Xinning and Leadbetter, Jared R. (2013) Genome-Wide Effects of Selenium and Translational Uncoupling on Transcription in the Termite Gut Symbiont Treponema primitia. mBio, 4 (6). Art. No. e00869-13. ISSN 2150-7511. PMCID PMC3892789. doi:10.1128/mBio.00869-13.

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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 (fdhF_Sec) 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. 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.

Item Type:Article
Related URLs:
URLURL TypeDescription 10.1128/mBio.00869-13DOIArticle CentralArticle
Rosenthal, Adam Z.0000-0002-6936-3665
Leadbetter, Jared R.0000-0002-7033-0844
Additional Information:© 2013 Matson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Received 10 October 2013; Accepted 15 October 2013; Published 12 November 2013. This work was supported by the DOE (DE-FG02-07ER64484), and the Center for Environmental Microbial Interactions (CEMI) at Caltech. We thank Igor Antoscheckhin and the Jacobs Genetics and Genomics Laboratory at Caltech for help with next-generation sequencing and Fabien Paulot for his help with RNA-Seq data analysis.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funding AgencyGrant Number
Department of Energy (DOE)DE-FG02-07ER64484
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Issue or Number:6
PubMed Central ID:PMC3892789
Record Number:CaltechAUTHORS:20140123-094750237
Persistent URL:
Official Citation:Matson EG, Rosenthal AZ, Zhang X, Leadbetter JR. 2013. Genome-wide effects of selenium and translational uncoupling on transcription in the termite gut symbiont Treponema primitia. mBio 4(6):e00869-13. doi:10.1128/mBio.00869-13.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:43485
Deposited On:23 Jan 2014 19:42
Last Modified:10 Nov 2021 16:38

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