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J. Biol. Chem., Vol. 282, Issue 10, 7690-7699, March 9, 2007

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Global Regulation of Photosynthesis and Respiration by FnrL

THE FIRST TWO TARGETS IN THE TETRAPYRROLE PATHWAY^*

From the Centre de Génétique Moléculaire CNRS (UPR-2167) Associéà l'Université Pierre et Marie Curie et Paris XI, Bâtiment 26, Avenue de la Terrasse, 91198 Gif sur Yvette Cedex, France

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 Mg²⁺-protoporphyrin monomethyl ester. Expression of both hemN and bchE in the FNR mutant restored synthesis of Mg²⁺-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.

Received for publication, June 22, 2006 , and in revised form, December 15, 2006.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY648960 [GenBank] .

^* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Table II and data.

¹ To whom correspondence should be addressed. Tel.: 33-1-69823165; Fax: 33-1-69823230; E-mail: souchane{at}cgm.cnrs-gif.fr.

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