RpoH2 sigma factor controls the photooxidative stress response in a non-photosynthetic rhizobacterium, Azospirillum brasilense Sp7

Kumar, Santosh; Kumar, Ashutosh; Mishra, Mukti Nath; Shukla, Mansi; Singh, Pradhyumna Kumar; Tripathi, Anil Kumar

doi:10.1099/mic.0.062380-0

Cited by 29 publications

(16 citation statements)

References 49 publications

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“…Recently, we reported that carotenoid synthesis is induced by light and regulated by a pair of ECF sigma factors (RpoE1 and RpoE2) in this bacterium (16)(17)(18). In addition, we have also shown that a heat shock sigma factor (RpoH2, or H ) is involved in the photooxidative stress response in this bacterium (19). These observations suggested that, besides RpoE1-ChrR1, RpoH2 might also be involved in the regulation of carotenoid biosynthesis in A. brasilense Sp7.…”

Section: Importancementioning

confidence: 73%

“…Identification of an RpoH-dependent promoter in the crtE2 upstream region prompted us to use the two-plasmid system to examine which of the five RpoH paralogs, encoded in the genome of A. brasilense (19), directly regulate crtE genes. Since the rpoH gene of E. coli is expressed under a heat shock condition, expression of ␤-galactosidase in E. coli DH5␣ can be observed only if an A. brasilense RpoH protein is able to drive the expression of lacZ from the crtE1 or crtE2 promoters.…”

Section: Resultsmentioning

confidence: 99%

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Carotenoid Biosynthetic Pathways Are Regulated by a Network of Multiple Cascades of Alternative Sigma Factors in Azospirillum brasilense Sp7

et al. 2016

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Carotenoids constitute an important component of the defense system against photooxidative stress in bacteria. In Azospirillum brasilense Sp7, a nonphotosynthetic rhizobacterium, carotenoid synthesis is controlled by a pair of extracytoplasmic function sigma factors (RpoEs) and their cognate zinc-binding anti-sigma factors (ChrRs). Its genome harbors two copies of the gene encoding geranylgeranyl pyrophosphate synthase (CrtE), the first critical step in the carotenoid biosynthetic pathway in bacteria. Inactivation of each of two crtE paralogs found in A. brasilense caused reduction in carotenoid content, suggesting their involvement in carotenoid synthesis. However, the effect of crtE1 deletion was more pronounced than that of crtE2 deletion. Out of the five paralogs of rpoH in A. brasilense, overexpression of rpoH1 and rpoH2 enhanced carotenoid synthesis. Promoters of crtE2 and rpoH2 were found to be dependent on RpoH2 and RpoE1, respectively. Using a two-plasmid system in Escherichia coli, we have shown that the crtE2 gene of A. brasilense Sp7 is regulated by two cascades of sigma factors: one consisting of RpoE1and RpoH2 and the other consisting of RpoE2 and RpoH1. In addition, expression of crtE1 was upregulated indirectly by RpoE1 and RpoE2. This study shows, for the first time in any carotenoid-producing bacterium, that the regulation of carotenoid biosynthetic pathway involves a network of multiple cascades of alternative sigma factors. Photosynthetic as well as nonphotosynthetic organisms encounter photooxidative stress caused by the generation of highly reactive singlet oxygen in the presence of light and oxygen. Singlet oxygen reacts with a wide range of cellular macromolecules, including proteins, lipids, DNA, and RNA, leading to the formation of reactive substances such as organic peroxides and sulfoxides (1). Mechanisms to cope with the photooxidative stress have been investigated in a range of photosynthetic and nonphotosynthetic microorganisms. These mechanisms include the use of quenchers, such as carotenoids, which interact either with excited photosensitizer molecules or singlet oxygen itself to prevent damage of cellular molecules (2). Carotenoids are a widely distributed class of structurally diverse yellow-, orange-, or red-pigmented compounds (tetraterpenoids) consisting of a polyene hydrocarbon chain derived from eight isoprene units. Modifications like cyclization and desaturations of C 40 backbone result in a variety of divergent chemical structures produced in eukaryotes as well as prokaryotes (3).Conversion of farnesyl pyrophosphate to geranylgeranyl pyrophosphate (GGPP) by GGPP synthase (CrtE) is a critical step before carotenoid biosynthesis begins in bacteria. The first two committed steps in the biosynthesis of carotenoids include conversion of GGPP into phytoene by a phytoene synthase (CrtB) followed by phytoene desaturation via phytoene dehydrogenase (CrtI). These three steps in the carotenoid biosynthetic pathway and associated enzymes are common in the carotenoid-produ...

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Section: Importancementioning

confidence: 73%

Section: Resultsmentioning

confidence: 99%

Carotenoid Biosynthetic Pathways Are Regulated by a Network of Multiple Cascades of Alternative Sigma Factors in Azospirillum brasilense Sp7

et al. 2016

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“…Azospirillum strains (and more particularly A. lipoferum 4B) harbor a remarkably high number of rpoH paralogues. While most of the Alphaproteobacteria harbor two copies of genes encoding RpoH sigma factors, this gene is present in five copies in the strains A. brasilense Sp7 and A. brasilense Sp245, whereas six copies are found in the A. lipoferum 4B genome (Wisniewski‐Dyé et al ., ; Kumar et al ., ). Interestingly, two copies ( rpoH4 and rpoH6 ) are similarly induced in sessile cells associated to artificial and rice roots (see above) and one copy is induced ( rpoH1 ) only in rice‐associated cells, suggesting that rpoH alleles are finely regulated during the adaptation of A. lipoferum 4B to rice roots.…”

Section: Resultsmentioning

confidence: 97%

Genome wide profiling ofAzospirillum lipoferum4B gene expression during interaction with rice roots

Drogue

Sanguin

Borland

et al. 2013

FEMS Microbiol Ecol

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Azospirillum-plant cooperation has been mainly studied from an agronomic point of view leading to a wide description of mechanisms implicated in plant growth-promoting effects. However, little is known about genetic determinants implicated in bacterial adaptation to the host plant during the transition from free-living to root-associated lifestyles. This study aims at characterizing global gene expression of Azospirillum lipoferum 4B following a 7-day-old interaction with two cultivars of Oryza sativa L. japonica (cv. Cigalon from which it was originally isolated, and cv. Nipponbare). The analysis was done on a whole genome expression array with RNA samples obtained from planktonic cells, sessile cells, and root-adhering cells. Root-associated Azospirillum cells grow in an active sessile-like state and gene expression is tightly adjusted to the host plant. Adaptation to rice seems to involve genes related to reactive oxygen species (ROS) detoxification and multidrug efflux, as well as complex regulatory networks. As revealed by the induction of genes encoding transposases, interaction with root may drive bacterial genome rearrangements. Several genes related to ABC transporters and ROS detoxification display cultivar-specific expression profiles, suggesting host specific adaptation and raising the question of A. lipoferum 4B/rice cv. Cigalon co-adaptation.

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“…Since oxidative and photooxidative stresses often lead to the denaturation of proteins, it was hypothesized that other paralogs might be involved in coping with stresses that cause protein denaturation. We have previously shown an involvement of RpoH2 in tolerating photooxidative stress in A. brasilense (36). In this study, the inability of rpoH3::km and rpoH5::km mutants to grow at 1 mM H 2 O 2 and severalfold induction of rpoH3 and rpoH5 transcripts by 1 mM H 2 O 2 indicated that both RpoH3 and RpoH5 were involved in coping with H 2 O 2 stress.…”

Section: Discussionmentioning

confidence: 48%

“…Both of these RpoE sigma factors respond to photooxidative or oxidative stress through their cognate anti-sigma factors, which possess redox-active zinc-binding motifs (2). Earlier, we had shown for A. brasilense that carotenoid biosynthesis, which confers protection against photooxidative stress (36)(37)(38), is regulated by two cascades of sigma factors, RpoE1¡RpoH2 and RpoE2¡RpoH1 (39). The genome of A. brasilense also encodes two copies of OxyR regulators, of which one is involved in the negative regulation of AhpC (40).…”

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confidence: 99%

Catalase Expression in Azospirillum brasilense Sp7 Is Regulated by a Network Consisting of OxyR and Two RpoH Paralogs and Including an RpoE1→RpoH5 Regulatory Cascade

Kumar

Singh

Dwivedi

et al. 2018

Appl Environ Microbiol

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The genome of encodes five RpoH sigma factors: two OxyR transcription regulators and three catalases. The aim of this study was to understand the role they play during oxidative stress and their regulatory interconnection. Out of the 5 paralogs of RpoH present in, inactivation of only renders heat sensitive. While transcript levels of were elevated by heat stress, those of and were upregulated by HO Catalase activity was upregulated in and its:: mutants in response to HO except in the case of the :: mutant, suggesting a role for RpoH5 in regulating inducible catalase. Transcriptional analysis of the ,I, and II genes revealed that the expression of and II was severely compromised in the:: and :: mutants, respectively. Regulation of andII by RpoH3 and RpoH5, respectively, was further confirmed in an two-plasmid system. Regulation ofII by OxyR2 was evident by a drastic reduction in growth, KatAII activity, and II:: expression in an :: mutant. This study reports the involvement of RpoH3 and RpoH5 sigma factors in regulating oxidative stress response in alphaproteobacteria. We also report the regulation of an inducible catalase by a cascade of alternative sigma factors and an OxyR. Out of the three catalases in , those corresponding to and II are regulated by RpoH3 and RpoH5, respectively. The expression ofII is regulated by a cascade of RpoE1→RpoH5 and OxyR2. analysis of the genome showed the presence of multiple paralogs of genes involved in oxidative stress response, which included 2 OxyR transcription regulators and 3 catalases. So far, and are known to harbor two paralogs of OxyR, and harbors three catalases. We do not yet know how the expression of multiple catalases is regulated in any bacterium. Here we show the role of multiple RpoH sigma factors and OxyR in regulating the expression of multiple catalases in Sp7. Our work gives a glimpse of systems biology of used for responding to oxidative stress.

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RpoH2 sigma factor controls the photooxidative stress response in a non-photosynthetic rhizobacterium, Azospirillum brasilense Sp7

Cited by 29 publications

References 49 publications

Carotenoid Biosynthetic Pathways Are Regulated by a Network of Multiple Cascades of Alternative Sigma Factors in Azospirillum brasilense Sp7

Carotenoid Biosynthetic Pathways Are Regulated by a Network of Multiple Cascades of Alternative Sigma Factors in Azospirillum brasilense Sp7

Genome wide profiling ofAzospirillum lipoferum4B gene expression during interaction with rice roots

Catalase Expression in Azospirillum brasilense Sp7 Is Regulated by a Network Consisting of OxyR and Two RpoH Paralogs and Including an RpoE1→RpoH5 Regulatory Cascade

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