Potential and Challenges of Improving Photosynthesis in Algae

Abstract

Sunlight energy largely exceeds the energy required by anthropic activities, and therefore its exploitation represents a major target in the field of renewable energies. The interest in the mass cultivation of green microalgae has grown in the last decades, as algal biomass could be employed to cover a significant portion of global energy demand. Advantages of microalgal vs. plant biomass production include higher light-use efficiency, efficient carbon capture and the valorization of marginal lands and wastewaters. Realization of this potential requires a decrease of the current production costs, which can be obtained by increasing the productivity of the most common industrial strains, by the identification of factors limiting biomass yield, and by removing bottlenecks, namely through domestication strategies aimed to fill the gap between the theoretical and real productivity of algal cultures. In particular, the light-to-biomass conversion efficiency represents one of the major constraints for achieving a significant improvement of algal cell lines. This review outlines the molecular events of photosynthesis, which regulate the conversion of light into biomass, and discusses how these can be targeted to enhance productivity through mutagenesis, strain selection or genetic engineering. This review highlights the most recent results in the manipulation of the fundamental mechanisms of algal photosynthesis, which revealed that a significant yield enhancement is feasible. Moreover, metabolic engineering of microalgae, focused upon the development of renewable fuel biorefineries, has also drawn attention and resulted in efforts for enhancing productivity of oil or isoprenoids.

Keywords: NPQ; RuBisCO; biomass productivity; complex PSII; light-harvesting; microalgae; photosynthesis; renewable energies; strain domestication.

Figure 1

Schematic representation of photosynthetic electron transport. Arrangement of Photosystem I (PSI), Photosystem II (PSII), cytochrome b6f and adenosine triphosphate (ATP) synthase complexes within the thylakoid membranes is shown. The light-driven water splitting reaction leads to O₂ evolution and originates linear electron transport (LET), indicated with black arrows, from water to nicotinamide adenine dinucleotide phosphate (NADP⁺), which is coupled to proton translocation from stroma into the luminal side of thylakoids during the light phase. The electrochemical gradient formed is used by the ATP synthase to produce ATP from Adenosine diphosphate (ADP) and Pi in the stroma. The NADPH and ATP formed during the light phase drive the Calvin–Benson–Bassham cycle reactions in the stroma. Two pathways of cyclic electron transport (CET) around PSI are indicated with red (Ferredoxin-dependent pathway) and green (NDA2-dependent pathway) arrows, respectively.

Figure 2

Supramolecular organization of PSII-LHCII and PSI-LHCI supercomplexes in the model alga Chlamydomonas reinhardtii. The schematic representations are based upon data from [33] for PSII-LHCII and from [36] for PSI-LHCI. The core complexes of both PSs are shown in light green while the antenna complexes are shown in dark green.

Figure 3

The Calvin–Benson–Bassham cycle (CBBc) reactions. The CBBc has three stages. In stage 1, the enzyme RuBisCO incorporates 3 CO₂ molecules into the 5-carbon sugar ribulose-1,5-bisphosphate (RuBP) to form 6 molecules of 3-phosphoglycerate (3-PGA). In stage 2, 6 molecules of 3-PGA are converted into 6 molecules of Glyceraldehyde-3-P (G3P) by using 6 molecules of ATP and 6 molecules of NADPH as reducing power. In stage 3, RuBP is regenerated so that the cycle can continue. Stage 3 includes a complex series of reactions combining 3-, 4-, 5-, 6-, and 7-carbon sugar phosphates, which are not explicitly shown in the diagram.

Figure 4

Scheme of long-term control mechanisms regulating light harvesting antenna size, as described in the model alga C. reinhardtii. (A) In low light conditions, carriers of the photosynthetic electron transport chain are oxidized, and all nuclear genes encoding LhcbMs isoforms associated to the PSII are expressed, except for the isoform 9. LhcbM-encoding mRNAs are translated in the cytosol, then targeted to the chloroplast and inserted in the thylakoid membranes. Under low light conditions, the translational repressor NAB1 is in a less active state. (B) In excess light conditions, ATP and NADPH produced by the light reactions exceed their consumption rate by the CBBc, and the overexcitation of PSII results in the release of reactive oxygen species (ROS). To alleviate excitation pressure, a remodelling of the antenna system is induced by slowing down the transcription of LhcbM genes. Once the translation of NAB1 is promoted, this subunit interacts with LhcbM-encoding mRNAs to form silent mRNA-ribonucleoprotein complexes. In contrast to all other isoforms, the expression of LhcbM9 and LhcsR3 proteins are induced.

Figure 5

Genes successfully targeted in C. reinhardtii or other species to improve photosynthetic productivity. Improvement of CO₂ fixation targets: RuBisCO, RuBisCO activase, LCI (Low-CO₂ Inducible protein), SBPase (sedoheptulose1,7-biphosphatase), FBPase (fructose-bisphosphate aldolase). Optical density reduction: cpSRP pathway (chloroplast signal recognition particle), TLA1 (Truncated Light-Harvesting Antenna 1), LhcbM, NAB1 (nucleic acid binding 1 protein) and CAO (Chlorophyllide a Oxygenase). Green arrows indicate the over-expressed genes, yellow arrows the down-regulated genes and red crosses indicate the knocked-down genes.