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Research Article

CceR and AkgR Regulate Central Carbon and Energy Metabolism in Alphaproteobacteria

Saheed Imam, Daniel R. Noguera, Timothy J. Donohue
Louis M. Weiss, Editor
Saheed Imam
aGraduate Program in Cellular and Molecular Biology, University of Wisconsin Madison, Madison, Wisconsin, USA
bDepartment of Bacteriology, University of Wisconsin Madison, Madison, Wisconsin, USA
cDOE Great Lakes Bioenergy Research Center, University of Wisconsin Madison, Madison, Wisconsin, USA
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Daniel R. Noguera
cDOE Great Lakes Bioenergy Research Center, University of Wisconsin Madison, Madison, Wisconsin, USA
dDepartment of Civil and Environmental Engineering, University of Wisconsin Madison, Madison, Wisconsin, USA
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Timothy J. Donohue
bDepartment of Bacteriology, University of Wisconsin Madison, Madison, Wisconsin, USA
cDOE Great Lakes Bioenergy Research Center, University of Wisconsin Madison, Madison, Wisconsin, USA
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  • ORCID record for Timothy J. Donohue
Louis M. Weiss
Albert Einstein College of Medicine
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DOI: 10.1128/mBio.02461-14
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ABSTRACT 

Many pathways of carbon and energy metabolism are conserved across the phylogeny, but the networks that regulate their expression or activity often vary considerably among organisms. In this work, we show that two previously uncharacterized transcription factors (TFs) are direct regulators of genes encoding enzymes of central carbon and energy metabolism in the alphaproteobacterium Rhodobacter sphaeroides. The LacI family member CceR (RSP_1663) directly represses genes encoding enzymes in the Entner-Doudoroff pathway, while activating those encoding the F1F0 ATPase and enzymes of the tricarboxylic acid (TCA) cycle and gluconeogenesis, providing a direct transcriptional network connection between carbon and energy metabolism. We identified bases that are important for CceR DNA binding and showed that DNA binding by this TF is inhibited by 6-phosphogluconate. We also showed that the GntR family TF AkgR (RSP_0981) directly activates genes encoding several TCA cycle enzymes, and we identified conditions where its activity is increased. The properties of single and double ΔCceR and ΔAkgR mutants illustrate that these 2 TFs cooperatively regulate carbon and energy metabolism. Comparative genomic analysis indicates that CceR and AkgR orthologs are found in other alphaproteobacteria, where they are predicted to have a conserved function in regulating central carbon metabolism. Our characterization of CceR and AkgR has provided important new insight into the networks that control central carbon and energy metabolism in alphaproteobacteria that can be exploited to modify or engineer new traits in these widespread and versatile bacteria.

IMPORTANCE To extract and conserve energy from nutrients, cells coordinate a set of metabolic pathways into integrated networks. Many pathways that conserve energy or interconvert metabolites are conserved across cells, but the networks regulating these processes are often highly variable. In this study, we characterize two previously unknown transcriptional regulators of carbon and energy metabolism that are conserved in alphaproteobacteria, a group of abundant, environmentally and biotechnologically important organisms. We identify the genes they regulate, the DNA sequences they recognize, the metabolite that controls the activity of one of the regulators, and conditions where they are required for growth. We provide important new insight into conserved cellular networks that can also be used to improve a variety of hosts for converting feedstock into valuable products.

FOOTNOTES

    • Received 21 December 2014
    • Accepted 29 December 2014
    • Published 3 February 2015
  • Copyright © 2015 Imam 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.

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CceR and AkgR Regulate Central Carbon and Energy Metabolism in Alphaproteobacteria
Saheed Imam, Daniel R. Noguera, Timothy J. Donohue
mBio Feb 2015, 6 (1) e02461-14; DOI: 10.1128/mBio.02461-14

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CceR and AkgR Regulate Central Carbon and Energy Metabolism in Alphaproteobacteria
Saheed Imam, Daniel R. Noguera, Timothy J. Donohue
mBio Feb 2015, 6 (1) e02461-14; DOI: 10.1128/mBio.02461-14
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