Posttranscriptional control of puc operon expression of B800-850 light-harvesting complex formation in Rhodobacter sphaeroides

Lee, J K; Kiley, Patricia J.; Kaplan, Samuel

doi:10.1128/jb.171.6.3391-3405.1989

Cited by 104 publications

(97 citation statements)

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“…Similarly, hemN was expressed aerobically at a low level with hemZ being off, but both showed increased expression when cells were shifted to anaerobic conditions as a result of the fact that both are under FnrL control (19,56). The expression level of pucC relative to pucBA is ϳ4 -8%, which is entirely consistent with the Northern hybridization results (33) and lacZ fusion studies (53) reported earlier, despite the fact that all of these genes reside in the pucBAC operon. Further, the expression of puhA (60) as well as pufBA (32) shows low expression under aerobic conditions as observed here, but both loci show increased expression as light intensity decreases.…”

Section: Effect Of Oxygen and Light On R Sphaeroides Transcriptomesupporting

confidence: 80%

“…However, these studies have been by necessity selective, and for the most part the overwhelming majority of these genetic elements comprising the photosynthetic lifestyle have never been investigated under the diverse environmental conditions described here. Photosynthesis Gene Cluster-As previously described for those genes encoding the apoproteins of the spectral complexes (19,32,33), there is a wealth of expression data, but for the most part the majority of the genes of the PS gene cluster of R. sphaeroides 2.4.1 have never been studied, except to note that their expression is higher under photosynthetic growth conditions relative to aerobic growth. In Fig.…”

Section: Effect Of Oxygen and Light On R Sphaeroides Transcriptomementioning

confidence: 99%

“…1 can be found at our web site (www.rhodobacter.org) and has been included here as supplementary data, available in the on-line version of this article. As described above there are many published studies that have followed, individually, the expression of a few, but not most of the genes encoding the photosystem in R. sphaeroides (32)(33)(34)(35)(36)(37), or genes encoding enzymes involved in CO 2 fixation (38, 39), nitrogen fixation (40), electron transport (41)(42)(43)(44)(45)(46), taxis (47,48), or assorted transcriptional regulators (16,49,50), etc., using more traditional approaches such as Northern hybridization, lacZ fusions, and even phoA fusions. However, these studies have been by necessity selective, and for the most part the overwhelming majority of these genetic elements comprising the photosynthetic lifestyle have never been investigated under the diverse environmental conditions described here.…”

Section: Effect Of Oxygen and Light On R Sphaeroides Transcriptomementioning

confidence: 99%

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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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Section: Effect Of Oxygen and Light On R Sphaeroides Transcriptomesupporting

confidence: 80%

Section: Effect Of Oxygen and Light On R Sphaeroides Transcriptomementioning

confidence: 99%

Section: Effect Of Oxygen and Light On R Sphaeroides Transcriptomementioning

confidence: 99%

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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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“…Radioactive probes were made by using highly purified plasmid DNA containing puf (pUI655), puc (pUI624) (29), cycA (pUI661), and puhA (pUI660) (26a) ( Table 1). All procedures have been described previously (14).…”

Section: Methodsmentioning

confidence: 99%

Oxygen-insensitive synthesis of the photosynthetic membranes of Rhodobacter sphaeroides: a mutant histidine kinase

Eraso¹,

Kaplan²

1995

J Bacteriol

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121

204

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Two new loci, prrB and prrC, involved in the positive regulation of photosynthesis gene expression in response to anaerobiosis, have been identified in Rhodobacter sphaeroides. prrB encodes a sensor histidine kinase that is responsive to the removal of oxygen and functions through the response regulator PrrA. Inactivation of prrB results in a substantial reduction of photosynthetic spectral complexes as well as in the inability of cells to grow photosynthetically at low to medium light intensities. Together, prrB and prrA provide the major signal involved in synthesis of the specialized intracytoplasmic membrane (ICM), harboring components essential to the light reactions of photosynthesis. Previously, J. K. Lee and S. Kaplan (J. Bacteriol. 174:1158-1171, 1992) identified a mutant which resulted in high-level expression of the puc operon, encoding the apoproteins giving rise to the B800-850 spectral complex, in the presence of oxygen as well as in the synthesis of the ICM under conditions of high oxygenation. This mutation is shown to reside in prrB, resulting in a leucine-to-proline change at position 78 in mutant PrrB (PRRB78). Measurements of mRNA levels in cells containing the prrB78 mutation support the idea that prrB is a global regulator of photosynthesis gene expression. Two additional mutants, PRRB1 and PRRB2, which make two truncated forms of the PrrB protein, possess substantially reduced amounts of spectral complexes. Although the precise role of prrC remains to be determined, evidence suggests that it too is involved in the regulatory cascade involving prrB and prrA. The genetic organization of the photosynthesis response regulatory (PRR) region is discussed.Rhodobacter sphaeroides is a purple, nonsulfur photoheterotrophic bacterium whose mode of growth depends on the concentration of oxygen in the surrounding environment (49). At high oxygen concentrations, R. sphaeroides grows chemoheterotrophically, and morphologically it resembles a typical gram-negative bacterium (3). Under low oxygen or anaerobiosis, the photosynthetic membrane system, designated the intracytoplasmic membrane (ICM), is induced; the ICM fills the interior of the cell, and its abundance is inversely related to the incident light intensity (25). The ICM contains all of the structural and functional components of the photosynthetic apparatus. Included are three distinct bacteriochlorophyll (Bchl) a pigment-protein complexes: the photochemical reaction center (RC) (36) and the two light-harvesting complexes, designated the B800-850 and B-875 spectral complexes (7, 9). When grown anaerobically in the dark, in the presence of alternative electron acceptors, the gratuitous synthesis of the ICM occurs (53).Lee and Kaplan (28) provided the first demonstration that a relatively simple switching mechanism must be involved in the repression of photosynthesis gene expression by oxygen in the genus Rhodobacter when they isolated the spontaneous mutant T 1a , which accumulates photosynthetic membranes in the presence of high oxygen. Subsequen...

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“…This study focuses on the mechanism of transcriptional control of the PS genes, in particular the ptlc operon, which encodes the structural polypeptides (Kiley & Kaplan, 1987) and assembly factor(s) (Gibson e t al., 1992;Lee et al, 1989b) for the LH I1 complex. Expression of most of the PS genes, includingptlc, depends on oxygen tension.…”

Section: Introductionmentioning

confidence: 99%

Isolation of regulatory mutants in photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1 and partial complementation of a PrrB mutant by the HupT histidine-kinase

Gomelsky

Kaplan

1995

Microbiology

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The photosynthetic bacterium Rhodobacter sphaemides responds to the transition from aerobiosis to anaerobic photosynthesis by increasing the expression of the photosynthesis genes. Mutants have been isolated based on their inability, following such a transition, to increase transcription of the puc operon encoding the apoproteins of the light-harvesting complex II. Mutant D5, a representative of one mutant class, described here, although remaining photosynthetically competent, produced only low levels of the photosynthetic spectral complexes. Complementation analysis revealed that either the gene for the photosynthesis response regulator prrA or the gene encoding its cognate sensor kinase, prrB, was capable of rescuing this mutant. However, partial complementation of this mutant was achieved by placing in trans additional copies of other defined genes from the cosmid library of R. sphaeroides. We describe this effect in detail, attributable to the hupT gene, which has been proposed to encode a histidine-kinase for the hydrogen uptake system in Rhodobacter capsulatus. The effect of HupT on the expression of the photosynthesis genes was mediated through PrrA and independent of a functioning hydrogen uptake system. Thus, we raise the possibility that HupT can participate in phosphorylation of the heterologous response regulator PrrA by so-called cross-talk and therefore partially compensate for the defect in the mutant described. The observation of cross-talk, together with the complementation analysis, allowed us to assign the original mutation to the prrB gene; this was confirmed by DNA sequencing. Analysis of cross-talk in the wild-type, prrB and prrA genetic backgrounds suggested that besides kinase activity, PrrB may possess phosphatase activity toward PrrA. We also report the cloning, organization and structure of some of the hup genes from R. sphaeroides and construction of a Hup-strain.

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Posttranscriptional control of puc operon expression of B800-850 light-harvesting complex formation in Rhodobacter sphaeroides

Cited by 104 publications

References 40 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

Oxygen-insensitive synthesis of the photosynthetic membranes of Rhodobacter sphaeroides: a mutant histidine kinase

Isolation of regulatory mutants in photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1 and partial complementation of a PrrB mutant by the HupT histidine-kinase

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