An ancient light-harvesting protein is critical for the regulation of algal photosynthesis

Abstract

Light is necessary for photosynthesis, but its absorption by pigment molecules such as chlorophyll can cause severe oxidative damage and result in cell death. The excess absorption of light energy by photosynthetic pigments has led to the evolution of protective mechanisms that operate on the timescale of seconds to minutes and involve feedback-regulated de-excitation of chlorophyll molecules in photosystem II (qE). Despite the significant contribution of eukaryotic algae to global primary production1, little is known about their qE mechanism, in contrast to that in flowering plants2,3. Here we show that a qE-deficient mutant of the unicellular green alga Chlamydomonas reinhardtii, npq4, lacks two of the three genes encoding LHCSR (formerly called LI818). This protein is an ancient member of the light-harvesting complex superfamily, and orthologues are found throughout photosynthetic eukaryote taxa4, except in red algae and vascular plants. The qE capacity of Chlamydomonas is dependent on environmental conditions and is inducible by growth under high light conditions. We show that the fitness of the npq4 mutant in a shifting light environment is reduced compared to wild-type cells, demonstrating that LHCSR is required for survival in a dynamic light environment. Thus, these data indicate that plants and algae use different proteins to dissipate harmful excess light energy and protect the photosynthetic apparatus from damage.

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Figure 1: NPQ of chlorophyll fluorescence in Chlamydomonas reinhardtii cells.
Figure 2: Survival of wild type (WT) and npq4 following a shift from a low-light-acclimated state to excess light for four hours.
Figure 3: Analysis of the LHCSR genes, LHCSR mRNA levels, and LHCSR protein accumulation in Chlamydomonas WT and npq4 mutant.

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Acknowledgements

We thank M. Guertin for providing the anti-LHCSR (LI818) antibody. This work was supported by grants from the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, US Department of Energy (K.K.N.), the Deutsche Forschungsgemeinschaft (M.H.), and the National Science Foundation (A.R.G.).

Author Contributions G.P., T.B.T., E.O., A.B., D.E. and K.K.N. performed research; G.P., A.R.G., M.H., and K.K.N. designed research; G.P., M.H. and K.K.N. analysed data and wrote the paper; all authors discussed the results and commented on the manuscript.

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Correspondence to Michael Hippler or Krishna K. Niyogi.

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Peers, G., Truong, T., Ostendorf, E. et al. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462, 518–521 (2009). https://doi.org/10.1038/nature08587

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