Identification and molecular genetic characterization of a sensor kinase responsible for coordinately regulating light harvesting and reaction center gene expression in response to anaerobiosis

Mosley, Chere S.; Suzuki, Jon Y.; Bauer, Carl E.

doi:10.1128/jb.176.24.7566-7573.1994

Cited by 127 publications

(173 citation statements)

References 38 publications

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“…The fact that substantial levels of Crt and Bchl are produced aerobically in PRRB78 indicates that in R. sphaeroides, the accumulation of these pigments and spectral complexes is under the direct control of prrB. In R. capsulatus, using bchC::lacZ and bchH::lacZ translational fusions (34,40), the role of regA and regB on pigment synthesis was not as apparent as observed here for R. sphaeroides.…”

Section: Discussioncontrasting

confidence: 50%

“…One of these genes, designated prrB, and its mutant allele prrB78 are shown to encode the histidine kinase responsive to anaerobiosis. This gene is similar to the recently identified regB gene in R. capsulatus (34). A mutant form of prrB responsible for its insensitivity to oxygen results in synthesis of the ICM in the presence of oxygen, providing the basis for the initial observation of Lee and Kaplan (28).…”

supporting

confidence: 61%

“…These genes are believed to play a role in cytochrome c oxidase subunit assembly in the mitochondria of this organism (39). The amino terminus of PrrB, which may comprise the sensing domain of the histidine kinase, was not found to be similar to any protein in GenBank except RegB, a histidine kinase from R. capsulatus whose sequence has been published recently (34). This domain contains six putative membrane-spanning regions, making PrrB most likely a protein anchored in the membrane at its amino-terminal half and with the kinase domain in the cytoplasm.…”

Section: Discussionmentioning

confidence: 99%

“…However, similarities to regions of genes which encode the membrane-spanning domains of several proteins were found, providing suggestive evidence that PrrB is anchored in the membrane, with six possible transmembrane domains. The regB gene, which encodes a histidine kinase with 58% identity and 75% similarity to prrB, has recently been identified in R. capsulatus (34). The amino terminus of PrrB is 70% similar and 48% identical to the amino terminus of RegB.…”

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confidence: 99%

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

Eraso¹,

Kaplan²

1995

J Bacteriol

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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Section: Discussioncontrasting

confidence: 50%

supporting

confidence: 61%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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

Eraso¹,

Kaplan²

1995

J Bacteriol

121

204

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“…The second gene, designated prrB (Eraso & Kaplan, 1995), encodes a cognate histidine-kinase for PrrA. In R. capsulattls an analogous two-component (RegA and RegB) regulatory system has also been described (Inoue et al, 1995 ;Mosley et al, 1994 ;Sganga & Bauer, 1992). PhillipsJones & Hunter (1994) cloned and sequenced a prrA/ regA homologue from yet another strain of R. sphaeroides and showed its ability to partially complement the R. capstllattls regA mutation.…”

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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Green life: Control of chloroplast gene transcription

Link

1996

BioEssays

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Chloroplasts and other plastids are plant cell organelles that account for major biochemical functions. They contain their own gene expression system but are integrated into the signaling network of the entire cell. Both nuclear and plastid genes are involved in chloroplast biogenesis, and the gene expression pathways both inside and outside the organelle are subject to developmental and environmental control. The plastid transcription apparatus reflects this general scheme, with a basic organelle‐encoded enzymatic machinery surrounded by factors that may be encoded by nuclear genes. Among the transcription regulatory mechanisms thought to play a role during plastid development are: (1) differential usage of promoter elements; (2) phosphorylation of transcription factors by a protein kinase, which is itself subject to phosphorylation and redox control; (3) dynamic changes in the composition of the transcription apparatus. In etioplasts, the dominating polymerase ‘B’ is a bacterial‐type enzyme, whereas the major chloroplast polymerase ‘A’ is a much larger enzyme reminiscent of those in the nucleus. These two enzyme forms may share common components and recruit others during development.

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Identification and molecular genetic characterization of a sensor kinase responsible for coordinately regulating light harvesting and reaction center gene expression in response to anaerobiosis

Cited by 127 publications

References 38 publications

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

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

Green life: Control of chloroplast gene transcription

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