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Title: Optimization of carbon and energy utilization through differential translational efficiency

Abstract

Control of translation is vital to all species. Here we employ a multi-omics approach to decipher condition-dependent translational regulation in the model acetogen Clostridium ljungdahlii. Integration of data from cells grown autotrophically or heterotrophically revealed that pathways critical to carbon and energy metabolism are under strong translational regulation. Major pathways involved in carbon and energy metabolism are not only differentially transcribed and translated, but their translational efficiencies are differentially elevated in response to resource availability under different growth conditions. We show that translational efficiency is not static and that it changes dynamically in response to mRNA expression levels. mRNAs harboring optimized 5'-untranslated region and coding region features, have higher translational efficiencies and are significantly enriched in genes encoding carbon and energy metabolism. In contrast, mRNAs enriched in housekeeping functions harbor sub-optimal features and have lower translational efficiencies. As a result, we propose that regulation of translational efficiency is crucial for effectively controlling resource allocation in energy-deprived microorganisms.

Authors:
 [1];  [1];  [1]; ORCiD logo [1];  [1];  [1];  [1]; ORCiD logo [1]
  1. Univ. of California San Diego, La Jolla, CA (United States)
Publication Date:
Research Org.:
Johns Hopkins Univ., Baltimore, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1483935
Grant/Contract Number:  
SC0012658
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Al-Bassam, Mahmoud M., Kim, Ji -Nu, Zaramela, Livia S., Kellman, Benjamin P., Zuniga, Cristal, Wozniak, Jacob M., Gonzalez, David J., and Zengler, Karsten. Optimization of carbon and energy utilization through differential translational efficiency. United States: N. p., 2018. Web. doi:10.1038/s41467-018-06993-6.
Al-Bassam, Mahmoud M., Kim, Ji -Nu, Zaramela, Livia S., Kellman, Benjamin P., Zuniga, Cristal, Wozniak, Jacob M., Gonzalez, David J., & Zengler, Karsten. Optimization of carbon and energy utilization through differential translational efficiency. United States. https://doi.org/10.1038/s41467-018-06993-6
Al-Bassam, Mahmoud M., Kim, Ji -Nu, Zaramela, Livia S., Kellman, Benjamin P., Zuniga, Cristal, Wozniak, Jacob M., Gonzalez, David J., and Zengler, Karsten. Fri . "Optimization of carbon and energy utilization through differential translational efficiency". United States. https://doi.org/10.1038/s41467-018-06993-6. https://www.osti.gov/servlets/purl/1483935.
@article{osti_1483935,
title = {Optimization of carbon and energy utilization through differential translational efficiency},
author = {Al-Bassam, Mahmoud M. and Kim, Ji -Nu and Zaramela, Livia S. and Kellman, Benjamin P. and Zuniga, Cristal and Wozniak, Jacob M. and Gonzalez, David J. and Zengler, Karsten},
abstractNote = {Control of translation is vital to all species. Here we employ a multi-omics approach to decipher condition-dependent translational regulation in the model acetogen Clostridium ljungdahlii. Integration of data from cells grown autotrophically or heterotrophically revealed that pathways critical to carbon and energy metabolism are under strong translational regulation. Major pathways involved in carbon and energy metabolism are not only differentially transcribed and translated, but their translational efficiencies are differentially elevated in response to resource availability under different growth conditions. We show that translational efficiency is not static and that it changes dynamically in response to mRNA expression levels. mRNAs harboring optimized 5'-untranslated region and coding region features, have higher translational efficiencies and are significantly enriched in genes encoding carbon and energy metabolism. In contrast, mRNAs enriched in housekeeping functions harbor sub-optimal features and have lower translational efficiencies. As a result, we propose that regulation of translational efficiency is crucial for effectively controlling resource allocation in energy-deprived microorganisms.},
doi = {10.1038/s41467-018-06993-6},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {Fri Oct 26 00:00:00 EDT 2018},
month = {Fri Oct 26 00:00:00 EDT 2018}
}

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Cited by: 23 works
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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
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The ribosome in action: Tuning of translational efficiency and protein folding: The Ribosome in Action
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Works referencing / citing this record:

Predicting proteome allocation, overflow metabolism, and metal requirements in a model acetogen
journal, March 2019


Predicting proteome allocation, overflow metabolism, and metal requirements in a model acetogen
journal, March 2019