by R. T. Sayre, S. Negi and G. Govindjee
ue to the overall low thermodynamic efficiency (1 – 4%) of photosynthesis and its impact on crop productivity, substantial efforts are being made to engineer photosynthesis to improve its light use and carbon capture efficiency to increase crop yields. The greatest potential for increasing photosynthetic efficiency may still be realized, however, by improving its light use efficiency.
In plants and algae, light saturates photosynthesis at approximately one fourth of full sunlight intensity. The excess light energy must then be dissipated through non-productive energy emission pathways often leading to substantial damage to the photosynthetic apparatus further reducing crop yields.
Earlier studies have shown that by reducing the optical cross section of the light-harvesting antenna complex, it is possible to increase photosynthetic efficiency and biomass yield in crops and algae by up to 40% when grown continuously in high light or in the field. In nature, however, light intensity varies substantially over the course of the day, with depth in the plant architecture or algal pond, and even seasonally.
Theoretically, a light-harvesting apparatus that could be continuously adjusted in size for differing light regimes could lead to further improvements in photosynthetic efficiency. Negi et al. (2020) have indeed described a strategy for the continuous light-mediated regulation of the light-harvesting antenna size in a green alga Chlamydomonas reinhardtii. This system is based on the post transcriptional regulation of chlorophyllide a oxygenase (CAO) protein levels and activity that catalyzes the synthesis of chlorophyll b (Chl b). Chl b is found only in the peripheral, nuclear-encoded light-harvesting complexes, and its selective reduction was shown to result in a corresponding decrease in the antenna size.
Using the light regulated nucleic acid binding protein 1(NAB1) translational repressor to control the expression of a gene fusion product between the 5’ NAB1 — binding element (LRE) and the CAO gene, Negi et al. (2020) demonstrated that Chlamydomonas LRE-CAO transformants lacking the wild-type CAO gene were able to continuously and reversibly alter the size of their light-harvesting complexes throughout the algal life cycle (see Figure 1).
In collaboration with Dr. Jun Minagawa’s laboratory, in Japan, they demonstrated that LRE-CAO transgenics having the highest photosynthetic efficiencies also had reduced levels of photoinhibition under high light and greater activity of non-photochemical quenching of the excited state of chlorophyll a. Further, they observed that the thylakoid membrane architecture was altered in structure such that the membrane thickness and lumen space were much more favorable for enhanced electron transport activity.
These results demonstrate that reduction in Chl b and light-harvesting antenna structure has pleiotropic effects on the photosynthetic apparatus. Significantly, when the LRE-CAO transgenics were grown as monocultures under conditions mimicking those of a commercial algal production pond, the transgenics had biomass yields that were more than two-fold higher than their wild-type parental strains. These are the greatest increases in biomass yield observed to date for algae engineered for improved photosynthetic efficiency.
An obvious concern is whether LRE-CAO transgenics would have an increased fitness advantage relative to wild-type algae in the wild. Early studies indicate that this is not likely to be the case. Thus, we have not engineered a “monster” strain. Chlamydomonas strains engineered to have fixed but optimal light-harvesting antenna sizes for biomass yield were less competitive than wild-type algae in mixed cultures due to the shading effect of the wild-type algae on transgenics with smaller but more efficient light-harvesting antenna complexes.
These results have clear implications for addressing global challenges for food and biomass production as well as carbon capture.