Dataset Information

Genomic reconstruction of ?54 regulons in Clostridiales.

ABSTRACT: BACKGROUND:The ?54 factor controls unique promoters and interacts with a specialized activator (enhancer binding proteins [EBP]) for transcription initiation. Although ?54 is present in many Clostridiales species that have great importance in human health and biotechnological applications, the cellular processes controlled by ?54 remain unknown. RESULTS:For systematic analysis of the regulatory functions of ?54, we performed comparative genomic reconstruction of transcriptional regulons of ?54 in 57 species from the Clostridiales order. The EBP-binding DNA motifs and regulated genes were identified for 263 EBPs that constitute 39 distinct groups. The reconstructed ?54 regulons contain the genes involved in fermentation and amino acid catabolism. The predicted ?54 binding sites in the genomes of Clostridiales spp. were verified by in vitro binding assays. To our knowledge, this is the first report about direct regulation of the Stickland reactions and butyrate and alcohols synthesis by ?54 and the respective EBPs. Considerable variations were demonstrated in the sizes and gene contents of reconstructed ?54 regulons between different Clostridiales species. It is proposed that ?54 controls butyrate and alcohols synthesis in solvent-producing species, regulates autotrophic metabolism in acetogenic species, and affects the toxin production in pathogenic species. CONCLUSIONS:This study reveals previously unrecognized functions of ?54 and provides novel insights into the regulation of fermentation and amino acid metabolism in Clostridiales species, which could have potential applications in guiding the treatment and efficient utilization of these species.

SUBMITTER: Nie X

PROVIDER: S-EPMC6615313 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Genomic reconstruction of σ<sup>54</sup> regulons in Clostridiales.

Nie Xiaoqun X Dong Wenyue W Yang Chen C

BMC genomics 20190709 1

<h4>Background</h4>The σ<sup>54</sup> factor controls unique promoters and interacts with a specialized activator (enhancer binding proteins [EBP]) for transcription initiation. Although σ<sup>54</sup> is present in many Clostridiales species that have great importance in human health and biotechnological applications, the cellular processes controlled by σ<sup>54</sup> remain unknown.<h4>Results</h4>For systematic analysis of the regulatory functions of σ<sup>54</sup>, we performed comparative ...[more]

PMID: 31288763

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Project description:BackgroundTranscriptional regulation by alternative sigma (σ) factors represents an important mechanism that allows bacteria to rapidly regulate transcript and protein levels in response to changing environmental conditions. While the role of the alternative σ factor σB has been comparatively well characterized in L. monocytogenes, our understanding of the roles of the three other L. monocytogenes alternative σ factors is still limited. In this study, we employed a quantitative proteomics approach using Isobaric Tags for Relative and Absolute Quantitation (iTRAQ) to characterize the L. monocytogenes σL, σH, and σC protein regulons. Proteomic comparisons used a quadruple alternative σ factor mutant strain (ΔBCHL) and strains expressing a single alternative σ factor (i.e., σL, σH, and σC; strains ΔBCH, ΔBCL, and ΔBHL) to eliminate potential redundancies between σ factors.ResultsAmong the three alternative σ factors studied here, σH provides positive regulation for the largest number of proteins, consistent with previous transcriptomic studies, while σL appears to contribute to negative regulation of a number of proteins. σC was found to regulate a small number of proteins in L. monocytogenes grown to stationary phase at 37°C. Proteins identified as being regulated by multiple alternative σ factors include MptA, which is a component of a PTS system with a potential role in regulation of PrfA activity.ConclusionsThis study provides initial insights into global regulation of protein production by the L. monocytogenes alternative σ factors σL, σH, and σC. While, among these σ factors, σH appears to positively regulate the largest number of proteins, we also identified PTS systems that appear to be co-regulated by multiple alternative σ factors. Future studies should not only explore potential roles of alternative σ factors in activating a "cascade" of PTS systems that potentially regulate PrfA, but also may want to explore the σL and σC regulons under different environmental conditions to identify conditions where these σ factors may regulate larger numbers of proteins or genes.

Project description:The canonical function of a bacterial sigma (σ) factor is to determine the gene specificity of the RNA polymerase (RNAP). In several diverse bacterial species, the σ54 factor uniquely confers distinct functional and regulatory properties on the RNAP. A hallmark feature of the σ54-RNAP is the obligatory requirement for an activator ATPase to allow transcription initiation. Different activator ATPases couple diverse environmental cues to the σ54-RNAP to mediate adaptive changes in gene expression. Hence, the genes that rely upon σ54 for their transcription have a wide range of different functions suggesting that the repertoire of functions performed by genes, directly or indirectly affected by σ54, is not yet exhaustive. By comparing the growth patterns of prototypical enteropathogenic, uropathogenic, and nonpathogenic Escherichia coli strains devoid of σ54, we uncovered that the absence of σ54 results in two differently sized colonies that appear at different times specifically in the uropathogenic E. coli (UPEC) strain. Notably, UPEC bacteria devoid of individual activator ATPases of the σ54-RNAP do not phenocopy the σ54 mutant strain. Thus, it seems that σ54's role as a determinant of uniform colony appearance in UPEC bacteria represents a putative non-canonical function of σ54 in regulating genetic information flow. IMPORTANCE RNA synthesis is the first step of gene expression. The multisubunit RNA polymerase (RNAP) is the central enzyme responsible for RNA synthesis in bacteria. The dissociable sigma (σ) factor subunit directs the RNAP to different sets of genes to allow their expression in response to various cellular needs. Of the seven σ factors in Escherichia coli and related bacteria, σ54 exists in a class of its own. This study has uncovered that σ54 is a determinant of the uniform growth of uropathogenic E. coli on solid media. This finding suggests a role for this σ54 in gene regulation that extends beyond its known function as an RNAP gene specificity factor.

Dataset Information

Genomic reconstruction of ?54 regulons in Clostridiales.

Publications

Genomic reconstruction of σ<sup>54</sup> regulons in Clostridiales.

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