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Binding Motifs in Bacterial Gene Promoters Modulate Transcriptional Effects of Global Regulators CRP and ArcA.

ABSTRACT: Bacterial gene regulation involves transcription factors (TF) that bind to DNA recognition sequences in operon promoters. These recognition sequences, many of which are palindromic, are known as regulatory elements or transcription factor binding sites (TFBS). Some TFs are global regulators that can modulate the expression of hundreds of genes. In this study we examine global regulator half-sites, where a half-site, which we shall call a binding motif (BM), is one half of a palindromic TFBS. We explore the hypothesis that the number of BMs plays an important role in transcriptional regulation, examining empirical data from transcriptional profiling of the CRP and ArcA regulons. We compare the power of BM counts and of full TFBS characteristics to predict induced transcriptional activity. We find that CRP BM counts have a nonlinear effect on CRP-dependent transcriptional activity and predict this activity better than full TFBS quality or location.

SUBMITTER: Leuze MR

PROVIDER: S-EPMC3370831 | biostudies-other | 2012

REPOSITORIES: biostudies-other

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Binding Motifs in Bacterial Gene Promoters Modulate Transcriptional Effects of Global Regulators CRP and ArcA.

Leuze Michael R MR Karpinets Tatiana V TV Syed Mustafa H MH Beliaev Alexander S AS Uberbacher Edward C EC

Gene regulation and systems biology 20120530

Bacterial gene regulation involves transcription factors (TF) that bind to DNA recognition sequences in operon promoters. These recognition sequences, many of which are palindromic, are known as regulatory elements or transcription factor binding sites (TFBS). Some TFs are global regulators that can modulate the expression of hundreds of genes. In this study we examine global regulator half-sites, where a half-site, which we shall call a binding motif (BM), is one half of a palindromic TFBS. We ...[more]

PMID: 22701314

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Project description:Microorganisms must respond to environmental changes to survive, often by controlling transcription initiation. Intermittent aeration during wastewater treatment presents a cyclically changing environment to which microorganisms must react. We used an intermittently aerated bioreactor performing partial nitritation and anammox (PNA) to investigate how the microbiome responds to recurring change. Meta-transcriptomic analysis revealed a dramatic disconnect between the relative DNA abundance and gene expression within the metagenome-assembled genomes (MAGs) of community members, suggesting the importance of transcriptional regulation in this microbiome. To explore how community members responded to cyclic aeration via transcriptional regulation, we searched for homologs of the catabolite repressor protein/fumarate and nitrate reductase regulatory protein (CRP/FNR) family of transcription factors (TFs) within the MAGs. Using phylogenetic analyses, evaluation of sequence conservation in important amino acid residues, and prediction of genes regulated by TFs in the MAGs, we identified homologs of the oxygen-sensing FNR in Nitrosomonas and Rhodocyclaceae, nitrogen-sensing dissimilative nitrate respiration regulator that responds to nitrogen species (DNR) in Rhodocyclaceae, and nitrogen-sensing nitrite and nitric oxide reductase regulator that responds to nitrogen species (NnrR) in Nitrospira MAGs. Our data also predict that CRP/FNR homologs in Ignavibacteria, Flavobacteriales, and Saprospiraceae MAGs sense carbon availability. In addition, a CRP/FNR homolog in a Brocadia MAG was most closely related to CRP TFs known to sense carbon sources in well-studied organisms. However, we predict that in autotrophic Brocadia, this TF most likely regulates a diverse set of functions, including a response to stress during the cyclic aerobic/anoxic conditions. Overall, this analysis allowed us to define a meta-regulon of the PNA microbiome that explains functions and interactions of the most active community members. IMPORTANCE Microbiomes are important contributors to many ecosystems, including ones where nutrient cycling is stimulated by aeration control. Optimizing cyclic aeration helps reduce energy needs and maximize microbiome performance during wastewater treatment; however, little is known about how most microbial community members respond to these alternating conditions. We defined the meta-regulon of a PNA microbiome by combining existing knowledge of how the CRP/FNR family of bacterial TFs respond to stimuli, with metatranscriptomic analyses to characterize gene expression changes during aeration cycles. Our results indicated that, for some members of the community, prior knowledge is sufficient for high-confidence assignments of TF function, whereas other community members have CRP/FNR TFs for which inferences of function are limited by lack of prior knowledge. This study provides a framework to begin elucidating meta-regulons in microbiomes, where pure cultures are not available for traditional transcriptional regulation studies. Defining the meta-regulon can help in optimizing microbiome performance.

Dataset Information

Binding Motifs in Bacterial Gene Promoters Modulate Transcriptional Effects of Global Regulators CRP and ArcA.

Publications

Binding Motifs in Bacterial Gene Promoters Modulate Transcriptional Effects of Global Regulators CRP and ArcA.

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