Genes involved in the biosynthesis of photosynthetic pigments in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina.

A pigment mutant strain of the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina BBS was isolated by plasposon mutagenesis. Nineteen open reading frame, most of which are thought to be genes involved in the biosynthesis of carotenoids, bacteriochlorophyll, and the photosynthetic reaction center, were identified surrounding the plasposon in a 22-kb-long chromosomal locus. The general arrangement of the photosynthetic genes was similar to that in other purple photosynthetic bacteria; however, the locations of a few genes occurring in this region were unusual. Most of the gene products showed the highest similarity to the corresponding proteins in Rubrivivax gelatinosus. The plasposon was inserted into the crtD gene, likely inactivating crtC as well, and the carotenoid composition of the mutant strain corresponded to the aborted spirilloxanthin pathway. Homologous and heterologous complementation experiments indicated a conserved function of CrtC and CrtD in the purple photosynthetic bacteria. The crtDC and crtE genes were shown to be regulated by oxygen, and a role of CrtJ in aerobic repression was suggested.

The photosynthetic apparatus in many purple bacteria consists of three kinds of pigment-protein complexes: two types of the light-harvesting antenna complex (LHI and LHII) absorb light and transfer the energy to the third complex, the reaction center (17). The pigment components of these complexes are essential for efficient photosynthetic performance.

In bacterial photosynthesis, carotenoids absorb light energy, participate in the assembly of the light-harvesting antenna complex (13), and protect the cells from photodamage (3).

Numerous pathways have been described for the biosynthesis of more than 100 known carotenoids in photosynthetic anoxygenic bacteria (30). The operons coding for the enzymes of specific carotenoid pathways in photosynthetic bacteria have been studied mainly in nonsulfur bacteria belonging to the α and β subclasses of proteobacteria (1, 10, 14, 16). Little is known about the genes of carotenoid biosynthesis in purple sulfur γ proteobacteria.

Oxygen and light are the main environmental factors affecting the transcription and assembly of the photosynthetic apparatus in Rhodobacter capsulatus and in Rhodobacter sphaeroides (19). In Rhodobacter sphaeroides the crt operons are repressed under aerobic conditions by PpsR (CrtJ is a counterpart in Rhodobacter capsulatus) (7, 20, 23). Thiocapsa roseopersicina BBS is a purple sulfur photosynthetic γ proteobacterium belonging to the family Chromatiaceae. It can be cultivated under photosynthetic anaerobic conditions and requires reduced sulfur compounds for growth. It also grows chemolithoautotrophically under dark, aerobic conditions. The members of the family Chromatiaceae have either spirilloxanthin (normal, unusual spirilloxanthin, and carotenal) or okenone carotenoid biosynthetic pathways (30). Spirilloxanthin was reported to be the major carotenoid in T. roseopersicina 1711 (DSM 217) (29). Here we describe the isolation and genetic analysis of a T. roseopersicina mutant strain with altered carotenoid content and the characterization of a 22-kb locus containing genes involved in pigment biosynthesis. The regulation of carotenoid biosynthesis genes in this purple sulfur bacterium is also discussed.