Light regulation of light‐harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae^†

Abstract

Summary One of the major factors limiting biomass productivity in algae is the low thermodynamic efficiency of photosynthesis. The greatest thermodynamic inefficiencies in photosynthesis occur during the conversion of light into chemical energy. At full sunlight the light‐harvesting antenna captures photons at a rate nearly 10 times faster than the rate‐limiting step in photosynthetic electron transport. Excess captured energy is dissipated by non‐productive pathways including the production of reactive oxygen species. Substantial improvements in photosynthetic efficiency have been achieved by reducing the optical cross‐section of the light‐harvesting antenna by selectively reducing chlorophyll b levels and peripheral light‐harvesting complex subunits. Smaller light‐harvesting antenna, however, may not exhibit optimal photosynthetic performance in low or fluctuating light environments. We describe a translational control system to dynamically adjust light‐harvesting antenna sizes for enhanced photosynthetic performance. By expressing a chlorophyllide a oxygenase (CAO) gene having a 5′ mRNA extension encoding a Nab1 translational repressor binding site in a CAO knockout line it was possible to continuously alter chlorophyll b levels and correspondingly light‐harvesting antenna sizes by light‐activated Nab1 repression of CAO expression as a function of growth light intensity. Significantly, algae having light‐regulated antenna sizes had substantially higher photosynthetic rates and two‐fold greater biomass productivity than the parental wild‐type strains as well as near wild‐type ability to carry out state transitions and non‐photochemical quenching. These results have broad implications for enhanced algae and plant biomass productivity.

Biology and biotechnological applications of microalgae and photosynthetic prokaryotes: part 2

“…At UIUC, we did several experiments together, using the green alga Chlamydomonas reinhardtii: (i) Together with Jin Xiong, Govindjee's PhD student, we showed the crucial importance of arginine-257 on D1 in the 'bicarbonate' effect (Gov's favourite; see Shevela et al 2012) on the electron acceptor side of Photosystem II (PS II), using newly constructed mutants and measurements on thermoluminescence (see Xiong, Minagawa et al 1998; it was just when Gov was a year away from retirement); and (ii) Together with Manfredo Seufferheld, a postdoc of Govindjee, we extended this work, with additional D1-R257 mutants, long after Gov's retirement, which provided a new insight not only on the 'bicarbonate' effect, but into the theory of how thermoluminescence comes about (Rose et al 2008). Our interaction was very recently renewed when Gov collaborated with Richard (Dick) Sayre's group; here, also using C. reinhardtii, Negi et al (2020) showed that by manipulating the 'antenna' system, we can increase the biomass of this alga by two-fold! At one point, Govindjee had visited RIKEN, and here, together, we did experiments on thermoluminescence, a phenomenon of great interest to Gov.…”

“…Professor Govindjee has made extensive contributions to photosynthesis research over a career spanning more than 60 years (Eaton-Rye 2013). Throughout his career Govindjee has worked with algae, beginning with his PhD thesis in 1960 focussing on the requirement for two pigment systems in the photosynthetic electron transport chain (Govindjee 1960) and continuing up to the present with a contribution investigating how regulating light-harvesting antenna size in green algae can substantially enhance photosynthetic efficiency and biomass yield (Negi et al 2020). Similarly, Professor Govindjee has regularly used cyanobacteria for photosynthesis research (Govindjee and Shevela 2011).…”

LETTER TO EDITORLight regulation of photosynthetic light harvesting doubles the biomass yield in the green alga Chlamydomonas

“…phyll (Chl) b. Chl b is found only in the peripheral, nuclearencoded 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 5ꞌ NAB1 -binding element (LRE) and the CAO gene (Mussgnug et al 2005), 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 Fig. 1).…”

“…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 (Mircovic et al 2017). Theoretically, a lightharvesting apparatus that could be continuously adjusted in size for differing light regimes could lead to further improvements in photosynthetic efficiency (Negi et al 2020). Negi et al (2020) have indeed described a strategy for the continuous light-mediated regulation of the lightharvesting antenna size in a green alga Chlamydomonas reinhardtii.…”

“…Theoretically, a lightharvesting apparatus that could be continuously adjusted in size for differing light regimes could lead to further improvements in photosynthetic efficiency (Negi et al 2020). Negi et al (2020) have indeed described a strategy for the continuous light-mediated regulation of the lightharvesting 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 chloro-light-harvesting antenna complexes (Henley et al 2013).…”