Far-Red Light Photoacclimation (FaRLiP) and Its Regulation in Cyanobacteria

Gaozhong Shena, Ming-Yang Hoa, Fei Gana, Chi Zhaoa, Nathan Souliera, Daniel P. Canniffea, Donald A. Bryanta,b,c
aDepartment of Biochemistry and Molecular Biology, The Pennsylvania State University, PA 16802 USA; bDepartment of Chemistry and Biochemistry, Montana State University, Bozeman, MT 59717 USA; cSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore

Cyanobacteria have evolved many different mechanisms to sense and respond to light in order to optimize light harvesting for photosynthesis. As demonstrated in six selected cyanobacterial strains that represent all five taxonomic sections, a wide spectrum of cyanobacteria inhabiting soils and benthic environments have evolved a novel acclimative response to far-red light (FRL), named Far-Red Light Photoacclimation (FaRLiP), to extend cyanobacterial light-harvesting beyond 700 nm. Grown under FRL conditions, each strain synthesized two new chlorophylls, Chl f and Chl d, in addition of Chl a. The FRL-induced pigments represented 8–10% and ~1% of the total Chl content, respectively. Isolation of the PSI, PSII and PBS complexes and spectroscopic and proteomic characterization, confirmed that cells grown in FRL extensively remodeled their photosynthetic apparatus using seventeen novel gene products from the FaRLiP gene cluster. The contribution of the FaRLiP-specific APC paralogs to the absorption in the 700-750 regions was also confirmed by heterologous protein expression and spectroscopic characterization. Through mutagenesis of the rfpA, rfpB and rfpC genes in two different cyanobacterial strains, we conclude that RfpA, RfpB and RfpC constitute a FRL-activated signal transduction cascade that is the master control switch for the FaRLiP response. The biosynthesis of Chl f and the remodeling of the core complexes of both photosystems and PBS provide the ability to utilize far-red light for photosynthesis.