Dual RpoH Sigma Factors and Transcriptional Plasticity in a Symbiotic Bacterium

Barnett, Melanie J.; Bittner, Alycia N.; Toman, Carol J.; Oke, Valerie; Long, Sharon R.

doi:10.1128/jb.00449-12

Cited by 65 publications

(129 citation statements)

References 68 publications

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“…An overlapping function of these RpoEs is manifested by RpoH1-and RpoH2-mediated regulation of a common gene (crtE2). A similar overlap of functions between RpoH1 and RpoH2 has also been demonstrated in R. sphaeroides (39) and Sinorhizobium meliloti (40). Furthermore, RpoE1-and -2-mediated regulation of RpoH4 and -5, which are not involved in carotenoid regulation, provides an insight into the utilization of RpoE1¡RpoH4 and RpoE2¡RpoH5 regulatory cascades for responding to other stresses, such as salinity and organic stresses, in which involvement of RpoE has been shown (25).…”

Section: Discussionmentioning

confidence: 75%

“…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).…”

Section: Importancementioning

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: Discussionmentioning

confidence: 75%

Section: Importancementioning

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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“…In addition to being critical for host plant invasion, EPS-I production is stimulated by low nitrogen, high phosphate, and stresses such as acid shock, heat shock, osmotic stress, and antimicrobial peptides (30)(31)(32)(33)(34)(35)(36). EPS-I protects S. meliloti against H 2 O 2 -dependent damage (37) and may also play a role in direct signaling to the plant (3,5).…”

mentioning

confidence: 99%

The Sinorhizobium meliloti SyrM Regulon: Effects on Global Gene Expression Are Mediated by syrA and nodD3

Barnett

Long

2015

J Bacteriol

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In Sinorhizobium meliloti, three NodD transcriptional regulators activate bacterial nodulation (nod) gene expression. NodD1 and NodD2 require plant compounds to activate nod genes. The NodD3 protein does not require exogenous compounds to activate nod gene expression; instead, another transcriptional regulator, SyrM, activates nodD3 expression. In addition, NodD3 can activate syrM expression. SyrM also activates expression of another gene, syrA, which when overexpressed causes a dramatic increase in exopolysaccharide production. In a previous study, we identified more than 200 genes with altered expression in a strain overexpressing nodD3. In this work, we define the transcriptomes of strains overexpressing syrM or syrA. The syrM, nodD3, and syrA overexpression transcriptomes share similar gene expression changes; analyses imply that nodD3 and syrA are the only targets directly activated by SyrM. We propose that most of the gene expression changes observed when nodD3 is overexpressed are due to NodD3 activation of syrM expression, which in turn stimulates SyrM activation of syrA expression. The subsequent increase in SyrA abundance results in broad changes in gene expression, most likely mediated by the ChvI-ExoS-ExoR regulatory circuit. IMPORTANCESymbioses with bacteria are prevalent across the animal and plant kingdoms. Our system of study, the rhizobium-legume symbiosis (Sinorhizobium meliloti and Medicago spp.), involves specific host-microbe signaling, differentiation in both partners, and metabolic exchange of bacterial fixed nitrogen for host photosynthate. During this complex developmental process, both bacteria and plants undergo profound changes in gene expression. The S. meliloti SyrM-NodD3-SyrA and ChvI-ExoS-ExoR regulatory circuits affect gene expression and are important for optimal symbiosis. In this study, we defined the transcriptomes of S. meliloti overexpressing SyrM or SyrA. In addition to identifying new targets of the SyrM-NodD3-SyrA regulatory circuit, our work further suggests how it is linked to the ChvI-ExoS-ExoR regulatory circuit. The symbiotic soil alphaproteobacterium Sinorhizobium meliloti forms nitrogen-fixing nodules on the roots of leguminous plants such as Medicago sativa (alfalfa) and Medicago truncatula (barrel medic). The earliest stages of the symbiosis involve an exchange of molecular signals: plant roots exude compounds that induce transcription of bacterial nod genes, which encode enzymes that synthesize lipochitooligosaccharide Nod factors (NF) (1, 2). These bacterial NF trigger early plant responses such as root hair curling, calcium spiking, and root cortical cell divisions to form the nodule organ (2). Bacteria trapped in curled root hairs penetrate the root hair through an infection thread (IT), an ingrowth of plant cell membrane and wall (3). As the IT elongates into the root, the bacteria at the tip are actively dividing.Bacterial polysaccharides, such as cyclic ␤-glucans and exopolysaccharide I (EPS-I; also known as succinoglycan), are essential for bacte...

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“…Like R. sphaeroides, the plant symbiont Sinorhizobium meliloti harbors two RpoH sigma factors. Both sigma factors play a role in stationary-phase survival (13), and the rpoHI and rpoHII mRNA levels increase during stationary phase (34).…”

Section: Resultsmentioning

confidence: 99%

An RpoHI-Dependent Response Promotes Outgrowth after Extended Stationary Phase in the Alphaproteobacterium Rhodobacter sphaeroides

et al. 2017

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Under unfavorable growth conditions, bacteria enter stationary phase and can maintain cell viability over prolonged periods with no increase in cell number. To obtain insights into the regulatory mechanisms that allow bacteria to resume growth when conditions become favorable again (outgrowth), we performed global transcriptome analyses at different stages of growth for the alphaproteobacterium Rhodobacter sphaeroides. The majority of genes were not differentially expressed across growth phases. After a short stationary phase (about 20 h after growth starts to slow down), only 7% of the genes showed altered expression (fold change of Ͼ1.6 or less than Ϫ1.6, corresponding to a log 2 fold change of Ͼ0.65 or less than Ϫ0.65, respectively) compared to expression at exponential phase. Outgrowth induced a distinct response in gene expression which was strongly influenced by the length of the preceding stationary phase. After a long stationary phase (about 64 h after growth starts to slow down), a much larger number of genes (15.1%) was induced in outgrowth than after a short stationary phase (1.7%). Many of those genes are known members of the RpoHI/RpoHII regulons and have established functions in stress responses. A main effect of RpoHI on the transcriptome in outgrowth after a long stationary phase was confirmed. Growth experiments with mutant strains further support an important function in outgrowth after prolonged stationary phase for the RpoHI and RpoHII sigma factors.IMPORTANCE In natural environments, the growth of bacteria is limited mostly by lack of nutrients or other unfavorable conditions. It is important for bacterial populations to efficiently resume growth after being in stationary phase, which may last for long periods. Most previous studies on growth-phase-dependent gene expression did not address outgrowth after stationary phase. This study on growth-phase-dependent gene regulation in a model alphaproteobacterium reveals, for the first time, that the length of the stationary phase strongly impacts the transcriptome during outgrowth. The alternative sigma factors RpoHI and RpoHII, which are important regulators of stress responses in alphaproteobacteria, play a major role during outgrowth following prolonged stationary phase. These findings provide the first insight into the regulatory mechanisms enabling efficient outgrowth.

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Dual RpoH Sigma Factors and Transcriptional Plasticity in a Symbiotic Bacterium

Cited by 65 publications

References 68 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

The Sinorhizobium meliloti SyrM Regulon: Effects on Global Gene Expression Are Mediated by syrA and nodD3

An RpoHI-Dependent Response Promotes Outgrowth after Extended Stationary Phase in the Alphaproteobacterium Rhodobacter sphaeroides

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