The role of the γ subunit in the photosystem of the lowest-energy phototrophs

Abstract

Purple phototrophic bacteria use a core photosystem consisting of light harvesting antenna complex 1 (LH1) surrounding the reaction centre (RC), which primarily absorbs far-red-near-infrared light and converts it to chemical energy. Species in the Blastochloris genus, which are able to use light >1000nm for photosynthesis, use bacteriochlorophyll (BChl) b rather than the more common BChl a as their major photopigment, and also uniquely assemble LH1 with an additional polypeptide subunit, LH1{gamma}, encoded by multiple open reading frames in their genomes. In order to assign a role to this subunit, we deleted the four LH1{gamma}-encoding genes in the model Blastochloris viridis. Interestingly, growth under halogen bulbs routinely used for cultivation of anoxygenic phototrophs yielded cells displaying an absorption maximum of 825 nm, similar to that of the RC complex without LH1, but growth under white light from fluorescent bulbs yielded cells with an absorption maximum at 972 nm. HPLC analysis of pigment composition and sucrose density gradient fractionation demonstrate that the mutant grown in white light assembles RC-LH1, albeit with an absorption maximum blue-shifted by 46 nm relative to the WT complex. Wavelengths between 900-1000 nm transmit poorly through the atmosphere due to strong absorption by water, thus our results provide an evolutionary rationale for the incorporation of the {gamma} subunit into the LH1 ring; this polypeptide red-shifts the absorption maximum of the complex to a range of the spectrum where the photons are of lower energy but are more abundant. Finally, we transformed the mutant with plasmids carrying genes encoding natural LH1{gamma} variants and demonstrate that the polypeptide found in the WT complex red-shifts absorption back to 1018 nm, but incorporation of a distantly-related variant results in only a moderate red-shift. This result suggests that tuning the absorption maximum of this organism is possible, and may permit light capture past the current low-energy limit of natural photosynthesis.