Fei Gan

Occurrence of Far-Red Light Photoacclimation (FaRLiP) in Diverse Cyanobacteria

Cyanobacteria have evolved a number of acclimation strategies to sense and respond to changing nutrient and light conditions. Leptolyngbya sp. JSC-1 was recently shown to photoacclimate to far-red light by extensively remodeling its photosystem (PS) I, PS II and phycobilisome complexes, thereby gaining the ability to grow in far-red light. A 21-gene photosynthetic gene cluster (rfpA/B/C, apcA2/B2/D2/E2/D3, psbA3/D3/C2/B2/H2/A4, psaA2/B2/L2/I2/F2/J2) that is specifically expressed in far-red light encodes the core subunits of the three major photosynthetic complexes. The growth responses to far-red light were studied here for five additional cyanobacterial strains, each of which has a gene cluster similar to that in Leptolyngbya sp. JSC-1. After acclimation all five strains could grow continuously in far-red light. Under these growth conditions each strain synthesizes chlorophylls d, f and a after photoacclimation, and each strain produces modified forms of PS I, PS II (and phycobiliproteins) that absorb light between 700 and 800 nm. We conclude that these photosynthetic gene clusters are diagnostic of the capacity to photoacclimate to and grow in far-red light. Given the diversity of terrestrial environments from which these cyanobacteria were isolated, it is likely that FaRLiP plays an important role in optimizing photosynthesis in terrestrial environments.

Adaptive and acclimative responses of cyanobacteria to far‐red light

Cyanobacteria use three major photosynthetic complexes, photosystem (PS) I, PS II and phycobilisomes, to harvest and convert sunlight into chemical energy. Until recently, it was generally thought that cyanobacteria only used light between 400 nm and 700 nm to perform photosynthesis. However, the discovery of chlorophyll (Chl) d in Acaryochloris marina and Chl f in Halomicronema hongdechloris showed that some cyanobacteria could utilize far-red light. The synthesis of Chl f (and Chl d) is part of an extensive acclimation process, far-red light photoacclimation (FaRLiP), which occurs in many cyanobacteria. Organisms performing FaRLiP contain a conserved set of 17 genes encoding paralogous subunits of the three major photosynthetic complexes. Far-red light photoacclimation leads to substantial remodelling of the photosynthetic apparatus and other changes in cellular metabolism through extensive changes in transcription. Far-red light photoacclimation appears to be controlled by a red/far-red photoreceptor, RfpA, as well as two response regulators (RfpB and RfpC), one of which is a DNA-binding protein. The remodelled photosynthetic complexes, including novel phycobiliproteins, absorb light above 700 nm and enable cells to grow in far-red light. A much simpler acclimation response, low-light photoacclimation (LoLiP), occurs in some cyanobacteria that contain the apcD4-apcB3-isiX cluster, which allows cells to grow under low light conditions.

RfpA, RfpB, and RfpC are the Master Control Elements of Far-Red Light Photoacclimation (FaRLiP)

Terrestrial cyanobacteria often occur in niches that are strongly enriched in far-red light (FRL; λ > 700 nm). Some cyanobacteria exhibit a complex and extensive photoacclimation response, known as FRL photoacclimation (FaRLiP). During the FaRLiP response, specialized paralogous proteins replace 17 core subunits of the three major photosynthetic complexes: Photosystem (PS) I, PS II, and the phycobilisome. Additionally, the cells synthesize both chlorophyll (Chl) f and Chl d. Using biparental mating from Escherichia coli, we constructed null mutants of three genes, rfpA, rfpB, and rfpC, in the cyanobacteria Chlorogloeopsis fritschii PCC 9212 and Chroococcidiopsis thermalis PCC 7203. The resulting mutants were no longer able to modify their photosynthetic apparatus to absorb FRL, were no longer able to synthesize Chl f, inappropriately synthesized Chl d in white light, and were unable to transcribe genes of the FaRLiP gene cluster. We conclude that RfpA, RfpB, and RfpC constitute a FRL-activated signal transduction cascade that is the master control switch for the FaRLiP response. FRL is proposed to activate (or inactivate) the histidine kinase activity of RfpA, which leads to formation of the active state of RfpB, the key response regulator and transcription activator. RfpC may act as a phosphate shuttle between RfpA and RfpB. Our results show that reverse genetics via conjugation will be a powerful approach in detailed studies of the FaRLiP response.