Global Regulation of Photosynthesis and Respiration by FnrL

Abstract

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...

Adaptation to Oxygen

“…In a high aeration context, reduction of oxygen tension starts with the bd quinol oxidase. When the oxygen tension is sufficiently low, activation of the transcription factor FnrL enhances the expression of cbb 3 oxidase (16). Complete reduction of O 2 via cbb 3 then allows inactivation of PpsR and full activation of the anaerobic regulator FnrL.…”

“…This circuit includes the two-component signal transduction system PrrBA (RegBA), the PpsR and FnrL transcriptional factors. So far, in R. gelatinosus only PpsR and FnrL were identified (16,20).…”

“…FnrL is a regulator that activates the expression of a variety of genes including photosynthesis genes in response to oxygen limitation in bacteria. Moreover, the FnrL null mutant in R. gelatinosus and R. sphaeroides are nonphotosynthetic (16,23 , cells resumed photosynthetic growth in liquid medium. This strain was still unable to grow by respiration, ruling out a possible genetic suppression of the phenotype.…”

“…This study focuses on the phototrophic Rubrivivax gelatinosus terminal oxidases and their requirement for photosynthetic and aerobic growth. We have previously detailed the AcsF/ BchE enzyme replacement and suggested a similar HemF to HemN replacement during the shift from aerobic to anaerobic environment to emphasize the O 2 -dependent and -independent metabolic networks (15,16). Here, we further investigate the problem of O 2 and photosynthesis (PS) 2 in this bacterium and show how the terminal oxidases expand the physiological range of O 2 environments under which R. gelatinosus and probably many other facultative phototrophs can carry out photosynthesis.…”

CtpA, a Copper-translocating P-type ATPase Involved in the Biogenesis of Multiple Copper-requiring Enzymes

“…Colonies with Cox activity turn blue after the addition of 10 l of the substrate. Staining of membranes for covalently bound heme with 3,3Ј,5,5Ј-tetramethylbenzidine was achieved as described in Ouchane et al (21).…”