Distribution and Origin of Oxygen-Dependent and Oxygen-Independent Forms of Mg-Protoporphyrin Monomethylester Cyclase among Phototrophic Proteobacteria

Abstract

ABSTRACTMagnesium-protoporphyrin IX monomethylester cyclase is one of the key enzymes of the bacteriochlorophyll biosynthesis pathway. There exist two fundamentally different forms of this enzyme. The oxygen-dependent form, encoded by the geneacsF, catalyzes the formation of the bacteriochlorophyll fifth ring using oxygen, whereas the oxygen-independent form encoded by the genebchEutilizes an oxygen atom extracted from water. The presence ofacsFandbchEgenes was surveyed in various phototrophicProteobacteriausing the available genomic data and newly designed degenerated primers. It was found that while the majority of purple nonsulfur bacteria contained both forms of the cyclase, the purple sulfur bacteria contained only the oxygen-independent form. All tested species of aerobic anoxygenic phototrophs containedacsFgenes, but some of them also retained thebchEgene. In contrast tobchEphylogeny, theacsFphylogeny was in good agreement with 16S inferred phylogeny. Moreover, the survey of the genome data documented that theacsFgene occupies a conserved position inside the photosynthesis gene cluster, whereas thebchElocation in the genome varied largely between the species. This suggests that the oxygen-dependent cyclase was recruited by purple phototrophic bacteria very early during their evolution. The primary sequence and immunochemical similarity with its cyanobacterial counterparts suggests thatacsFmay have been acquired byProteobacteriavia horizontal gene transfer from cyanobacteria. The acquisition of the gene allowed purple nonsulfur phototrophic bacteria to proliferate in the mildly oxygenated conditions of the Proterozoic era.