Regulation of 5-aminolevulinic acid synthesis in Rhodobacter sphaeroides 2.4.1: the genetic basis of mutant H-5 auxotrophy

Zeilstra-Ryalls, Jill H.; Kaplan, Samuel

doi:10.1128/jb.177.10.2760-2768.1995

Cited by 34 publications

(28 citation statements)

References 23 publications

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“…Recently, studies have revealed that the role of oxygen in ICM formation is the result of the actions of key regulatory pathways, including the cbb 3 terminal oxidase-PrrBA pathway (6 -10), the PpsR-AppA repressor-anti-repressor pathway (11)(12)(13)(14), and the FnrL pathway (15,16). Light intensity has a somewhat more subtle effect on photosynthetically growing cells, whereby the cellular levels of ICM are inversely related to light intensity and the composition of the ICM is differentially altered with changing light intensity (1,17).…”

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Effects of Oxygen and Light Intensity on Transcriptome Expression in Rhodobacter sphaeroides 2.4.1

Roh

Smith

Kaplan

2004

Journal of Biological Chemistry

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The roles of oxygen and light on the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1 have been well studied over the past 50 years. More recently, the effects of oxygen and light on gene regulation have been shown to involve the interacting redox chains present in R. sphaeroides under diverse growth conditions, and many of the redox carriers comprising these chains have been well studied. However, the expression patterns of those genes encoding these redox carriers, under aerobic and anaerobic photosynthetic growth, have been less well studied. Here, we provide a transcriptional analysis of many of the genes comprising the photosynthesis lifestyle, including genes corresponding to many of the known regulatory elements controlling the response of this organism to oxygen and light. The observed patterns of gene expression are evaluated and discussed in light of our knowledge of the physiology of R. sphaeroides under aerobic and photosynthetic growth conditions. Finally, this analysis has enabled to us go beyond the traditional patterns of gene expression associated with the photosynthesis lifestyle and to consider, for the first time, the full complement of genes responding to oxygen, and variations in light intensity when growing photosynthetically. The data provided here should be considered as a first step in enabling one to model electron flow in R. sphaeroides 2.4

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Effects of Oxygen and Light Intensity on Transcriptome Expression in Rhodobacter sphaeroides 2.4.1

Roh

Smith

Kaplan

2004

Journal of Biological Chemistry

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“…A model derived from early studies mainly based on analyses of the Fnr mutants and promoter activity measurements in R. sphaeroides was proposed (31,32). From these studies it was inferred that Fnr acts as a positive regulator of genes for heme biosynthesis, 5-aminolevulinic acid synthase (hemA) and the coprophorphyrinogen III oxidases (hemZ and hemN), for bacteriochlorophyll synthesis bchEJG operon, and for the pucBA operon encoding the polypeptides of the light-harvesting complex LHII (11,14,(32)(33)(34). In this organism the fnrL gene was shown to regulate respiratory genes including the ccoNOQP operon encoding the microaerobic cbb 3 cytochrome oxidase and the rdxBHIS genes involved in cytochrome cbb 3 biogenesis (35,36).…”

Section: Discussionmentioning

confidence: 99%

“…Taken together, these data may explain the photosynthesis-competent phenotype of FNR mutant in R. capsulatus. Zeilstra-Ryalls and Kaplan (34) proposed that the tetrapyrrole and bacteriochlorophyll biosynthetic genes hemA, hemZ, hemN, and bchE may require increased expression under photosynthetic conditions in R. sphaeroides. Later, Oh et al (31) have shown that bchE and hemN expression requires FnrL.…”

Section: Discussionmentioning

confidence: 99%

Global Regulation of Photosynthesis and Respiration by FnrL

Ouchane

Picaud

Therizols

et al. 2007

Journal of Biological Chemistry

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Fnr is a regulator that controls the expression of a variety of genes in response to oxygen limitation in bacteria. To assess the role of Fnr in photosynthesis in Rubrivivax gelatinosus, a strain carrying a null mutation in fnrL was constructed. It was unable to grow anaerobically in the light, but, intriguingly, it was able to produce photosynthetic complexes under high oxygenation conditions. The mutant lacked all c-type cytochromes normally detectable in microaerobically-grown wild type cells and accumulated coproporphyrin III. These data suggested that the pleiotropic phenotype observed in FNR is primarily due to the control at the level of the HemN oxygen-independent coproporphyrinogen III dehydrogenase. hemN expression in trans partially suppressed the FNR phenotype, as it rescued heme and cytochrome syntheses. Nevertheless, these cells were photosynthetically deficient, and pigment analyses showed that they were blocked at the level of Mg 2؉ -protoporphyrin monomethyl ester. Expression of both hemN and bchE in the FNR mutant restored synthesis of Mg 2؉ -protochlorophyllide. We, therefore, conclude that FnrL controls respiration by regulating hemN expression and controls photosynthesis by regulating both hemN and bchE expression. A comprehensive picture of the control points of microaerobic respiration and photosynthesis by FnrL is provided, and the prominent role of this factor in activating alternative gene programs after reduction of oxygen tension in facultative aerobes is discussed.Anoxygenic photosynthetic bacteria can develop the required machinery for growth under aerobic respiration, anaerobic respiration, or photosynthesis under anaerobiosis and light. This faculty requires tight control to ensure production of the required complexes and rapid adaptation to changes in environmental conditions. Under anaerobiosis and light, purple bacteria perform anoxygenic photosynthesis on the basis of a bacteriochlorophyll-mediated process. It takes place within the membrane-bound photosynthetic apparatus composed of pigment-protein complexes (reaction center (RC) 2 and light harvesting (LH)) and involves membrane cytochromes. Synthesis of tetrapyrroles (heme and chlorophyll) is then a crucial process necessary for photosynthesis and respiratory growth of these organisms. Heme synthesis and its regulation have been studied in many organisms (for review, see Refs. 1-4). A key step in this pathway corresponds to the conversion of coproporphyrinogen III to protoporphyrinogen IX. In facultative aerobic prokaryotes, two structurally different enzymes catalyze this reaction depending on the oxygenation level. Under high oxygenation, the oxidation is catalyzed in Escherichia coli by the oxygen-dependent coproporphyrinogen III oxidase (HemF). Under anaerobiosis, an oxygen-independent coproporphyrinogen III dehydrogenase (HemN) is required (5, 6). Bacteriochlorophyll synthesis and its regulation have also been studied in many phototrophs (for review, see Ref. 7). A key step in the chlorophyll pathway in facultative aer...

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“…The wild-type prrA gene was amplified from purified genomic DNA (1) using primers PrrA5ЈUP (5Ј-GGCAAAGCCCTCGCTCGTC-3Ј) and PrrA3ЈDOWN (5Ј-CTT GATCGCAGCCTCGAACCAG-3Ј) and ligated into the EcoRV site of pUI1087 (40) to create plasmid pBRO86. This plasmid was then used for oligonucleotide-directed mutagenesis with primer PrrAD63KUP (5Ј-GCCTATGCA GTGGTGAAGCTGCGGCTCGAGGAC-3Ј) and the complementary primer, PrrAD63KDOWN, to create a mutant prrA gene coding for the D63K aminoacid-substituted protein.…”

Section: Methodsmentioning

confidence: 99%

“…At the same time, appropriate levels of heme and vitamin B 12 must also be maintained. This radical change in tetrapyrrole biosynthesis is enabled in part by an increase in ALA formation (23), and with respect to oxygen control we have found that among the ALA synthase genes present in this organism, alterations in hemA expression are responsible (38,40). Therefore, investigations of hemA regulation should provide insights into the mechanisms of oxygen control in the cell.…”

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confidence: 99%

Regulation of the Rhodobacter sphaeroides 2.4.1 hemA Gene by PrrA and FnrL

Ranson-Olson

Zeilstra-Ryalls

2008

J Bacteriol

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Part of the oxygen responsiveness of Rhodobacter sphaeroides 2.4.1 tetrapyrrole production involves changes in transcription of the hemA gene, which codes for one of two isoenzymes catalyzing 5-aminolevulinic acid synthesis. Regulation of hemA transcription from its two promoters is mediated by the DNA binding proteins FnrL and PrrA. The two PrrA binding sites, binding sites I and II, which are located upstream of the more-5 hemA promoter (P1), are equally important to transcription under aerobic conditions, while binding site II is more important under anaerobic conditions. By using phosphoprotein affinity chromatography and immunoblot analyses, we showed that the phosphorylated PrrA levels in the cell increase with decreasing oxygen tensions. Then, using both in vivo and in vitro methods, we demonstrated that the relative affinities of phosphorylated and unphosphorylated PrrA for the two binding sites differ and that phosphorylated PrrA has greater affinity for site II. We also showed that PrrA regulation is directed toward the P1 promoter. We propose that the PrrA component of anaerobic induction of P1 transcription is attributable to higher affinity of phosphorylated PrrA than of unphosphorylated PrrA for binding site II. Anaerobic activation of the more-3 hemA promoter (P2) is thought to involve FnrL binding to an FNR consensuslike sequence located upstream of the P2 promoter, but the contribution of FnrL to P1 induction may be indirect since the P1 transcription start is within the putative FnrL binding site. We present evidence suggesting that the indirect action of FnrL works through PrrA and discuss possible mechanisms.

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Regulation of 5-aminolevulinic acid synthesis in Rhodobacter sphaeroides 2.4.1: the genetic basis of mutant H-5 auxotrophy

Cited by 34 publications

References 23 publications

Effects of Oxygen and Light Intensity on Transcriptome Expression in Rhodobacter sphaeroides 2.4.1

Effects of Oxygen and Light Intensity on Transcriptome Expression in Rhodobacter sphaeroides 2.4.1

Global Regulation of Photosynthesis and Respiration by FnrL

Regulation of the Rhodobacter sphaeroides 2.4.1 hemA Gene by PrrA and FnrL

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