A global signal transduction system regulates aerobic and anaerobic CO2 fixation in Rhodobacter sphaeroides

Abstract

Complementation of a mutant of Rhodobacter sphaeroides defective in photosynthetic CO 2 reduction led to the identification of a gene which encodes a protein that is related to a class of sensor kinases involved in bacterial signal transduction. The nucleotide sequence and deduced amino acid sequence led to the finding that the gene which complemented the mutant is the regB (prrB) gene, previously isolated from both R. sphaeroides and Rhodobacter capsulatus and shown to regulate the anaerobic expression of structural genes required for the synthesis of the reaction center and light-harvesting systems of these organisms. The current investigation indicates that in addition to its role in the regulation of photosystem biosynthesis, regB (prrB) of R. sphaeroides is intimately involved in the positive regulation of the cbb I and cbb II Calvin cycle CO 2 fixation operons. In addition to regulating the expression of structural genes encoding enzymes of the primary pathway for CO 2 fixation in R. sphaeroides, regB was also found to be required for the expression of a gene(s) important for the putative alternative CO 2 fixation pathway(s) of this organism. A mutation in regB also blocked expression of structural genes of the cbb regulon in a strain of R. sphaeroides capable of aerobic CO 2 -dependent growth in the dark. It is thus apparent that regB is part of a two-component system and encodes a sensor kinase involved in the global regulation of both anoxygenic light-dependent-and oxygenic light-independent CO 2 fixation as well as anoxygenic photosystem biosynthesis.Rhodobacter sphaeroides is a nonsulfur purple bacterium capable of both anoxygenic photosynthetic growth and vigorous aerobic growth in the dark. Under photolithoautotrophic growth conditions, this organism may be cultured with H 2 being used as an electron donor and CO 2 being used as the electron acceptor and sole carbon source. R. sphaeroides also employs various organic compounds as electron donors and major carbon sources (photoheterotrophic growth), and several organic acids, such as malate, succinate, and butyrate, are especially well suited for this growth mode. Although the role of CO 2 fixation is diminished under photoheterotrophic conditions, CO 2 is still assimilated primarily through the Calvin cycle (33). Thus, ribulose 1,5-bisphosphate carboxylase-oxygenase (Rubisco), the key enzyme of the primary CO 2 fixation pathway (14), is essential for photosynthetic growth when CO 2 is the major carbon source or prime electron acceptor. Interestingly, there are two distinct forms of Rubisco in R. sphaeroides, each of which, by itself, is capable of supporting photolithoautotrophic and photoheterotrophic growth (7). When the form I and form II Rubisco genes are both deleted, as in the case of R. sphaeroides 16 (a Rubisco double deletion mutant, cbbL cbbS cbbM), the organism is no longer capable of photolithoautotrophic growth in an H 2 -CO 2 atmosphere; under photoheterotrophic growth conditions in the presence of malate, growth is also impossible unl...

A periplasmic, α-type carbonic anhydrase from Rhodopseudomonas palustris is essential for bicarbonate uptake

“…sphaeroides. In these bacteria the RegA\RegB system was found to regulate the aerobic and anaerobic expression of genes encoding enzymes of primary and alternative CO # fixation and integrates photosynthesis and nitrogen fixation (Qian & Tabita, 1996 ;Joshi & Tabita, 1996). However, a RegA-like consensus recognition motif (Du et al, 1998) was not found in the sequence of acaP, nor upstream of the coding region, which suggests that a different regulatory system is involved.…”

Combining microarray and genomic data to predict DNA binding motifs

“…In addition to regulating photosynthesis-gene expression, PrrA acts as a global regulator, affecting the expression of genes encoding electron-transport components, genes involved in CO 2 and N 2 fixation, and genes involved in hydrogen oxidation, among others (Elsen et al, 2004;Joshi & Tabita, 1996;Qian & Tabita, 1996). Although the importance of the role played by PrrA in gene regulation is clear, the DNA sequence to which it binds remains poorly defined.…”

Regulation of synthesis of pyruvate carboxylase in the photosynthetic bacterium Rhodobacter capsulatus

“…Our results suggest that a similar regulatory mechanism(s) which monitors the ratio of intracellular concentrations of pyruvate and C 4 dicarboxylates may be involved in the control of PC synthesis in R. capsulatus. Recently, RegB-RegA, a global two-component regulatory system, was identified in R. capsulatus and R. sphaeroides and shown to be involved in the control of carbon (CO 2 ) metabolism and photosystem biosynthesis (25,31). However, this regulatory system does not appear to be involved in the regulation of PC synthesis, since a regB mutant showed wild-type levels of PC protein when grown under light anaerobic conditions (47a).…”