Functional diversification of two bilin reductases for light perception and harvesting in unique cyanobacterium Acaryochloris marina MBIC 11017

Bilin pigments play important roles for both light perception and harvesting in cyanobacteria by binding to cyanobacteriochromes (CBCRs) and phycobilisomes (PBS), respectively. Among various cyanobacteria, Acaryochloris marina MBIC 11017 (A. marina 11017) exceptionally uses chlorophyll d as the main photosynthetic pigment absorbing longer wavelength light than the canonical pigment, chlorophyll a, indicating existence of a system to sense longer wavelength light than others. On the other hand, A. marina 11017 has the PBS apparatus to harvest short-wavelength orange light, similar to most cyanobacteria. Thus, A. marina 11017 might sense longer wavelength light and harvest shorter wavelength light by using bilin pigments. Phycocyanobilin (PCB) is the main bilin pigment of both systems. Phycocyanobilin:ferredoxin oxidoreductase (PcyA) catalyzes PCB synthesis from biliverdin via the intermediate 18(1),18(2)-dihydrobiliverdin (18(1),18(2)-DHBV), resulting in the stepwise shortening of the absorbing wavelengths. In this study, we found that A. marina 11017 exceptionally encodes two PcyA homologs, AmPcyAc and AmPcyAp. AmPcyAc is encoded on the main chromosome with most photoreceptor genes, whereas AmPcyAp is encoded on a plasmid with PBS-related genes. High accumulation of 18(1),18(2)-DHBV for extended periods was observed during the reaction catalyzed by AmPcyAc, whereas 18(1),18(2)-DHBV was transiently accumulated for a short period during the reaction catalyzed by AmPcyAp. CBCRs could sense longer wavelength far-red light through 18(1),18(2)-DHBV incorporation, whereas PBS could only harvest orange light through PCB incorporation, suggesting functional diversification of PcyA as AmPcyAc and AmPcyAp to provide 18(1),18(2)-DHBV and PCB to the light perception and harvesting systems, respectively.