Comparative genomics and evolution of regulons of the LacI-family transcription factors

Ravcheev, Dmitry A.; Khoroshkin, Matvei S.; Laikova, Olga N.; Tsoy, Olga V.; Sernova, Natalia V.; Petrova, Svetlana A.; Rakhmaninova, Aleksandra B.; Novichkov, Pavel S.; Gelfand, Mikhail S.; Rodionov, Dmitry A.

doi:10.3389/fmicb.2014.00294

Comparative genomics and evolution of regulons of the LacI-family transcription factors

Journal Article · Wed Jun 11 00:00:00 EDT 2014 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2014.00294· OSTI ID:1628110

Ravcheev, Dmitry A. ^[1]; Khoroshkin, Matvei S. ^[2]; Laikova, Olga N. ^[2]; Tsoy, Olga V. ^[3]; Sernova, Natalia V. ^[2]; Petrova, Svetlana A. ^[3]; Rakhmaninova, Aleksandra B. ^[4]; Novichkov, Pavel S. ^[5]; Gelfand, Mikhail S. ^[2]; Rodionov, Dmitry A. ^[6]

Russian Academy of Sciences (RAS), Moscow (Russian Federation); DOE/OSTI
Russian Academy of Sciences (RAS), Moscow (Russian Federation)
Russian Academy of Sciences (RAS), Moscow (Russian Federation); Moscow State University, Moscow (Russian Federation)
Moscow State University, Moscow (Russian Federation)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Russian Academy of Sciences (RAS), Moscow (Russian Federation); Sanford-Burnham Medical Research Institute, La Jolla, CA (United States)

DNA-binding transcription factors (TFs) are essential components of transcriptional regulatory networks in bacteria. LacI-family TFs (LacI-TFs) are broadly distributed among certain lineages of bacteria. The majority of characterized LacI-TFs sense sugar effectors and regulate carbohydrate utilization genes. The comparative genomics approaches enable in silico identification of TF-binding sites and regulon reconstruction. To study the function and evolution of LacI-TFs, we performed genomics-based reconstruction and comparative analysis of their regulons. For over 1300 LacI-TFs from over 270 bacterial genomes, we predicted their cognate DNA-binding motifs and identified target genes. Using the genome context and metabolic subsystem analyses of reconstructed regulons, we tentatively assigned functional roles and predicted candidate effectors for 78 and 67% of the analyzed LacI-TFs, respectively. Nearly 90% of the studied LacI-TFs are local regulators of sugar utilization pathways, whereas the remaining 125 global regulators control large and diverse sets of metabolic genes. The global LacI-TFs include the previously known regulators CcpA in Firmicutes, FruR in Enterobacteria, and PurR in Gammaproteobacteria, as well as the three novel regulators—GluR, GapR, and PckR—that are predicted to control the central carbohydrate metabolism in three lineages of Alphaproteobacteria. Phylogenetic analysis of regulators combined with the reconstructed regulons provides a model of evolutionary diversification of the LacI protein family. The obtained genomic collection of in silico reconstructed LacI-TF regulons in bacteria is available in the RegPrecise database (http://regprecise.lbl.gov). It provides a framework for future structural and functional classification of the LacI protein family and identification of molecular determinants of the DNA and ligand specificity. The inferred regulons can be also used for functional gene annotation and reconstruction of sugar catabolic networks in diverse bacterial lineages.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Russian Foundation for Basic Research

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1628110

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 5; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Transcriptional Regulation of Central Carbon and Energy Metabolism in Bacteria by Redox-Responsive Repressor Rex Ravcheev, D. A.; Li, X.; Latif, H. Journal of Bacteriology, Vol. 194, Issue 5 https://doi.org/10.1128/JB.06412-11	journal	December 2011
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Transcriptional Profiling of Caulobacter crescentus during Growth on Complex and Minimal Media Hottes, Alison K.; Meewan, Maliwan; Yang, Desiree Journal of Bacteriology, Vol. 186, Issue 5 https://doi.org/10.1128/JB.186.5.1448-1461.2004	journal	March 2004
Functional Domains of the Bacillus subtilis Transcription Factor AraR and Identification of Amino Acids Important for Nucleoprotein Complex Assembly and Effector Binding Franco, Irina Saraiva; Mota, Luís Jaime; Soares, Cláudio Manuel Journal of Bacteriology, Vol. 188, Issue 8 https://doi.org/10.1128/JB.188.8.3024-3036.2006	journal	April 2006
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Using orthologous and paralogous proteins to identify specificity determining residues Mirny, Leonid A.; Gelfand, Mikhail S. Genome Biology, Vol. 3, Issue 3, preprint0002.1 https://doi.org/10.1186/gb-2002-3-3-preprint0002	journal	January 2002
Computational Reconstruction of Iron- and Manganese-Responsive Transcriptional Networks in α-Proteobacteria Rodionov, Dmitry A.; Gelfand, Mikhail S.; Todd, Jonathan D. PLoS Computational Biology, Vol. 2, Issue 12 https://doi.org/10.1371/journal.pcbi.0020163	journal	January 2006
Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima Rodionov, Dmitry A.; Rodionova, Irina A.; Li, Xiaoqing Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00244	journal	January 2013
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent ETH Zurich https://doi.org/10.3929/ethz-b-000025281	text	January 2010
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Oxford University Press https://doi.org/10.5167/uzh-155669	text	January 2010
Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus K., Seidl,; S., Müller,; P., François, BioMed Central https://doi.org/10.5167/uzh-19891	text	January 2009

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59 BASIC BIOLOGICAL SCIENCES
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regulons
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Comparative genomics and evolution of regulons of the LacI-family transcription factors

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