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Regulation of hydrogen peroxide-dependent gene expression in Rhodobacter sphaeroides: regulatory functions of OxyR.

ABSTRACT: Genome-wide transcriptome profiling was used to reveal hydrogen peroxide (H(2)O(2))-dependent regulatory mechanisms in the facultatively photosynthetic bacterium Rhodobacter sphaeroides. In this study we focused on the role of the OxyR protein, a known regulator of the H(2)O(2) response in bacteria. The transcriptome profiles of R. sphaeroides wild-type and oxyR mutant strains that were exposed to 1 mM H(2)O(2) for 7 min or were not exposed to H(2)O(2) were analyzed. Three classes of OxyR-dependent genes were identified based on their expression patterns in the wild type of oxyR mutant strains with differing predicted roles of oxidized and reduced OxyR as activators of transcription. DNA binding studies revealed that OxyR binds upstream of class I genes, which are induced by H(2)O(2) and exhibit similar basal levels of expression in the wild-type and oxyR mutant strains. The effect of OxyR on class II genes, which are also induced by H(2)O(2) but exhibit significantly lower basal levels of expression in the wild-type strain than in the mutant, is indirect. Interestingly, reduced OxyR also activates expression of few genes (class III). The role of reduced OxyR as an activator is shown for the first time. Our data reveal that the OxyR-mediated response is fast and transient. In addition, we found that additional regulatory pathways are involved in the H(2)O(2) response.

SUBMITTER: Zeller T

PROVIDER: S-EPMC1913319 | biostudies-literature | 2007 May

REPOSITORIES: biostudies-literature

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Regulation of hydrogen peroxide-dependent gene expression in Rhodobacter sphaeroides: regulatory functions of OxyR.

Zeller Tanja T Mraheil Mobarak A MA Moskvin Oleg V OV Li Kuanyu K Gomelsky Mark M Klug Gabriele G

Journal of bacteriology 20070309 10

Genome-wide transcriptome profiling was used to reveal hydrogen peroxide (H(2)O(2))-dependent regulatory mechanisms in the facultatively photosynthetic bacterium Rhodobacter sphaeroides. In this study we focused on the role of the OxyR protein, a known regulator of the H(2)O(2) response in bacteria. The transcriptome profiles of R. sphaeroides wild-type and oxyR mutant strains that were exposed to 1 mM H(2)O(2) for 7 min or were not exposed to H(2)O(2) were analyzed. Three classes of OxyR-depend ...[more]

PMID: 17351037

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Project description:BACKGROUND: High intracellular levels of unbound iron can contribute to the production of reactive oxygen species (ROS) via the Fenton reaction, while depletion of iron limits the availability of iron-containing proteins, some of which have important functions in defence against oxidative stress. Vice versa increased ROS levels lead to the damage of proteins with iron sulphur centres. Thus, organisms have to coordinate and balance their responses to oxidative stress and iron availability. Our knowledge of the molecular mechanisms underlying the co-regulation of these responses remains limited. To discriminate between a direct cellular response to iron limitation and indirect responses, which are the consequence of increased levels of ROS, we compared the response of the ?-proteobacterium Rhodobacter sphaeroides to iron limitation in the presence or absence of oxygen. RESULTS: One third of all genes with altered expression under iron limitation showed a response that was independent of oxygen availability. The other iron-regulated genes showed different responses in oxic or anoxic conditions and were grouped into six clusters based on the different expression profiles. For two of these clusters, induction in response to iron limitation under oxic conditions was dependent on the OxyR regulatory protein. An OxyR mutant showed increased ROS production and impaired growth under iron limitation. CONCLUSION: Some R. sphaeroides genes respond to iron limitation irrespective of oxygen availability. These genes therefore reflect a "core iron response" that is independent of potential ROS production under oxic, iron-limiting conditions. However, the regulation of most of the iron-responsive genes was biased by oxygen availability. Most strikingly, the OxyR-dependent activation of a subset of genes upon iron limitation under oxic conditions, including many genes with a role in iron metabolism, revealed that elevated ROS levels were an important trigger for this response. OxyR thus provides a regulatory link between the responses to oxidative stress and to iron limitation in R. sphaeroides.

Project description:BackgroundThe genus Rhodobacter contains purple nonsulfur bacteria found mostly in freshwater environments. Representative strains of two Rhodobacter species, R. capsulatus and R. sphaeroides, have had their genomes fully sequenced and both have been the subject of transcriptional profiling studies. Gene co-expression networks can be used to identify modules of genes with similar expression profiles. Functional analysis of gene modules can then associate co-expressed genes with biological pathways, and network statistics can determine the degree of module preservation in related networks. In this paper, we constructed an R. capsulatus gene co-expression network, performed functional analysis of identified gene modules, and investigated preservation of these modules in R. capsulatus proteomics data and in R. sphaeroides transcriptomics data.ResultsThe analysis identified 40 gene co-expression modules in R. capsulatus. Investigation of the module gene contents and expression profiles revealed patterns that were validated based on previous studies supporting the biological relevance of these modules. We identified two R. capsulatus gene modules preserved in the protein abundance data. We also identified several gene modules preserved between both Rhodobacter species, which indicate that these cellular processes are conserved between the species and are candidates for functional information transfer between species. Many gene modules were non-preserved, providing insight into processes that differentiate the two species. In addition, using Local Network Similarity (LNS), a recently proposed metric for expression divergence, we assessed the expression conservation of between-species pairs of orthologs, and within-species gene-protein expression profiles.ConclusionsOur analyses provide new sources of information for functional annotation in R. capsulatus because uncharacterized genes in modules are now connected with groups of genes that constitute a joint functional annotation. We identified R. capsulatus modules enriched with genes for ribosomal proteins, porphyrin and bacteriochlorophyll anabolism, and biosynthesis of secondary metabolites to be preserved in R. sphaeroides whereas modules related to RcGTA production and signalling showed lack of preservation in R. sphaeroides. In addition, we demonstrated that network statistics may also be applied within-species to identify congruence between mRNA expression and protein abundance data for which simple correlation measurements have previously had mixed results.

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Regulation of hydrogen peroxide-dependent gene expression in Rhodobacter sphaeroides: regulatory functions of OxyR.

Publications

Regulation of hydrogen peroxide-dependent gene expression in Rhodobacter sphaeroides: regulatory functions of OxyR.

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