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Exceptional Quantum Efficiency Powers Biomass Production in Halotolerant Algae Picochlorum sp.^

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Abstract

The green algal genus Picochlorum is of biotechnological interest because of its robust response to multiple environmental stresses. We compared the metabolic performance of P. SE3 and P. oklahomense to diverse microbial phototrophs and observed exceptional performance of photosystem II (PSII) in light energy conversion in both Picochlorum species. The quantum yield (QY) for O2 evolution is the highest of any phototroph yet observed, 32% (20%) by P. SE3 (P. okl) when normalized to total PSII subunit PsbA (D1) protein, and 80% (75%) normalized per active PSII, respectively. Three factors contribute: (1) an efficient water oxidizing complex (WOC) with the fewest photochemical misses of any organism; (2) faster reoxidation of reduced (PQH2)B in P. SE3 than in P. okl. (period-2 Fourier amplitude); and (3) rapid reoxidation of the plastoquinol pool by downstream electron carriers (Cyt b6f/PETC) that regenerates PQ faster in P. SE3. This performance gain is achieved without significant residue changes around the QB site and thus points to a pull mechanism involving faster PQH2 reoxidation by Cyt b6f/PETC that offsets charge recombination. This high flux in P. SE3 may be explained by genomically encoded plastoquinol terminal oxidases 1 and 2, whereas P. oklahomense has neither. Our results suggest two distinct types of PSII centers exist, one specializing in linear electron flow and the other in PSII-cyclic electron flow. Several amino acids within D1 differ from those in the low-light-descended D1 sequences conserved in Viridiplantae, and more closely match those in cyanobacterial high-light D1 isoforms, including changes near tyrosine Yz and a water/proton channel near the WOC. These residue changes may contribute to the exceptional performance of Picochlorum at high-light intensities by increasing the water oxidation efficiency and the electron/proton flux through the PSII acceptors (QAQB).

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Data availability

All data used to generate the figures in this paper and its supporting information are available from C.G., F.F., and G.C.D. on request.

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Acknowledgements

This work was funded by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy (Grant DE-FG02-10ER16195), and the NIFA-USDA Hatch program (NJ01180). We thank Drs. G.K. Kumaraswamy, Anagha Krishnan, Xiao Qian, and Matt Posewitz for input and advice.

Funding

U.S. Department of Energy, DE-FG02-10ER16195, DE-FG02-10ER16195, National Institute of Food and Agriculture, NJ01180.

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Authors and Affiliations

  1. Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, New Brunswick, NJ, 08854, USA

    Colin Gates, Gennady Ananyev & G. Charles Dismukes

  2. Department of Biochemistry and Microbiology, Rutgers, The State University of New Jersey, New Brunswick, NJ, 08854, USA

    Fatima Foflonker

  3. Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, New Brunswick, NJ, 08854, USA

    Colin Gates, Gennady Ananyev & G. Charles Dismukes

  4. Department of Computational Biology and Molecular Biophysics Rutgers, The State University of New Jersey, New Brunswick, NJ, 08854, USA

    Colin Gates & Debashish Bhattacharya

  5. Department of Chemistry and Biochemistry, Loyola University Chicago, Chicago, IL, 60660, USA

    Colin Gates

  6. Department of Biological Sciences, Clark Atlanta University, Atlanta, GA, 30314, USA

    Fatima Foflonker

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G.C.D. and D.B. conceptualized the manuscript, provided direction, and acquired funding. C.G. and G.A. developed methods. G.A., C.G., and F.F. performed experiments and generated data. C.G., G.A., and F.F. analyzed data. C.G., G.C.D., F.F., and G.A. drafted the manuscript. All authors reviewed and edited the manuscript.

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^This manuscript is dedicated to the memory of Kenneth Sauer, a pioneer in photosynthesis research and a dedicated mentor committed to the personal lives and career aspirations of his students.

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Gates, C., Ananyev, G., Foflonker, F. et al. Exceptional Quantum Efficiency Powers Biomass Production in Halotolerant Algae Picochlorum sp.^. Photosynth Res (2024). https://doi.org/10.1007/s11120-024-01075-9

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