Functional diversification of ROK-family transcriptional regulators of sugar catabolism in the Thermotogae phylum

Kazanov, Marat D.; Li, Xiaoqing; Gelfand, Mikhail S.; Osterman, Andrei L.; Rodionov, Dmitry A.

doi:10.1093/nar/gks1184

Functional diversification of ROK-family transcriptional regulators of sugar catabolism in the Thermotogae phylum

Journal Article · Sun Dec 02 00:00:00 EST 2012 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gks1184· OSTI ID:1904608

Kazanov, Marat D. ^[1]; Li, Xiaoqing ^[2]; Gelfand, Mikhail S. ^[3]; Osterman, Andrei L. ^[2]; Rodionov, Dmitry A. ^[4]

Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States); Russian Academy of Sciences (RAS), Moscow (Russian Federation); Sanford-Burnham Medical Research Inst., La Jolla, CA (United States)
Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States)
Russian Academy of Sciences (RAS), Moscow (Russian Federation)
Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States); Russian Academy of Sciences (RAS), Moscow (Russian Federation)

Large and functionally heterogeneous families of transcription factors have complex evolutionary histories. What shapes specificities toward effectors and DNA sites in paralogous regulators is a fundamental question in biology. Bacteria from the deep-branching lineage Thermotogae possess multiple paralogs of the repressor, open reading frame, kinase (ROK) family regulators that are characterized by carbohydrate-sensing domains shared with sugar kinases. We applied an integrated genomic approach to study functions and specificities of regulators from this family. A comparative analysis of 11 Thermotogae genomes revealed novel mechanisms of transcriptional regulation of the sugar utilization networks, DNA-binding motifs and specific functions. Reconstructed regulons for seven groups of ROK regulators were validated by DNA-binding assays using purified recombinant proteins from the model bacterium Thermotoga maritima. All tested regulators demonstrated specific binding to their predicted cognate DNA sites, and this binding was inhibited by specific effectors, mono- or disaccharides from their respective sugar catabolic pathways. By comparing ligand-binding domains of regulators with structurally characterized kinases from the ROK family, we elucidated signature amino acid residues determining sugar-ligand regulator specificity. Observed correlations between signature residues and the sugar-ligand specificities provide the framework for structure functional classification of the entire ROK family.

View Accepted Manuscript (DOE)

Research Organization:: Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States); University of California, San Diego, CA (United States)

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

Grant/Contract Number:: FG02-08ER64686; SC0004999

OSTI ID:: 1904608

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 2 Vol. 41; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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