Abstract
Bacterial response to nitric oxide (NO) is of major importance since NO is an obligatory intermediate of the nitrogen cycle. Transcriptional regulation of the dissimilatory nitric oxides metabolism in bacteria is diverse and involves FNR-like transcription factors HcpR, DNR, and NnrR; two-component systems NarXL and NarQP; NO-responsive activator NorR; and nitrite-sensitive repressor NsrR. Using comparative genomics approaches, we predict DNA-binding motifs for these transcriptional factors and describe corresponding regulons in available bacterial genomes. Within the FNR family of regulators, we observed a correlation of two specificity-determining amino acids and contacting bases in corresponding DNA recognition motif. Highly conserved regulon HcpR for the hybrid cluster protein and some other redox enzymes is present in diverse anaerobic bacteria, including Clostridia, Thermotogales, and delta-proteobacteria. NnrR and DNR control denitrification in alpha- and beta-proteobacteria, respectively. Sigma-54-dependent NorR regulon found in some gamma- and beta-proteobacteria contains various enzymes involved in the NO detoxification. Repressor NsrR, which was previously known to control only nitrite reductase operon in Nitrosomonas spp., appears to be the master regulator of the nitric oxides' metabolism, not only in most gamma- and beta-proteobacteria (including well-studied species such as Escherichia coli), but also in Gram-positive Bacillus and Streptomyces species. Positional analysis and comparison of regulatory regions of NO detoxification genes allows us to propose the candidate NsrR-binding motif. The most conserved member of the predicted NsrR regulon is the NO-detoxifying flavohemoglobin Hmp. In enterobacteria, the regulon also includes two nitrite-responsive loci, nipAB (hcp-hcr) and nipC (dnrN), thus confirming the identity of the effector, i.e. nitrite. The proposed NsrR regulons in Neisseria and some other species are extended to include denitrification genes. As the result, we demonstrate considerable interconnection between various nitrogen-oxides-responsive regulatory systems for the denitrification and NO detoxification genes and evolutionary plasticity of this transcriptional network.
Highlights
Interconversion of nitrogen species between a number of redox states forms the biogeochemical nitrogen cycle, which has multiple environmental impacts and industrial applications
HcpR: Recognition Motifs and Core Regulon A member of the CRP/FNR family of transcription factors, HcpR has been initially identified as the regulator of the hcp gene encoding the hybrid cluster protein and the frdX encoding a ferredoxin-like protein in the Desulfovibrio species, anaerobic metal-reducing d-proteobacteria [33]
As the analysis of the regulator multiple alignment revealed a substitution in the helix-turnhelix motif involved in DNA recognition that could cause this change, and since the considered species have multiple hcp and frdX paralogs, we applied the motif detection procedure to a set of corresponding upstream regions and obtained a new FNR-like palindromic motif with consensus sequence wyTTGACnnnnGTCAArw, which has a notable distinction from the CRP-like motif in the third position
Summary
Interconversion of nitrogen species between a number of redox states forms the biogeochemical nitrogen cycle, which has multiple environmental impacts and industrial applications. Bacteria can utilize soluble nitrogen oxides, nitrate and nitrite, as terminal electron acceptors in oxygen-limiting conditions. Two dissimilar pathways of nitrate respiration, ammonification and denitrification, involve formation of a common intermediate, nitrite, but end in different products, ammonia and gaseous nitrogen oxides or dinitrogen, respectively (Figure 1). Nitrite is formed by one of three different types of nitrate reductases: soluble assimilatory Nas, membrane-associated respiratory Nar, and periplasmic dissimilatory Nap. The step of ammonification is conversion of nitrite into ammonia by either respiratory cytochrome c nitrite reductase NrfA or detoxifying sirohemecontaining enzyme NirBD [1]. During denitrification, nitrite is reduced to nitric oxide (NO), nitrous oxide, and, dinitrogen, using nitrogen oxide reductases NirK (or NirS), NorB, and NosZ, respectively [2]
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