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Biochemical and spectroscopic characterizations of the oligomeric antenna of the coral symbiotic Symbiodiniaceae Fugacium kawagutii

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Abstract

Light-harvesting antennas in photosynthesis capture light energy and transfer it to the reaction centers (RCs) where photochemistry takes place. The sustainable growth of the reef-building corals relies on a constant supply of the photosynthates produced by the endosymbiotic dinoflagellate, belonging to the family of Symbiodiniaceae. The antenna system in this group consists of the water-soluble peridinin-chlorophyll a-protein (PCP) and the intrinsic membrane chlorophyll a-chlorophyll c2-peridinin protein complex (acpPC). In this report, a nonameric acpPC is reported in a dinoflagellate, Fugasium kawagutii (formerly Symbiodinium kawagutii sp. CS-156). We found that extensive biochemical purification altered the oligomerization states of the initially isolated nonameric acpPC. The excitation energy transfer pathways in the acpPC nonamer and its variants were studied using time-resolved fluorescence and time-resolved absorption spectroscopic techniques at 77 K. Compared to the well-characterized trimeric acpPC, the nonameric acpPC contains an 11 nm red-shifted terminal energy emitter and substantially altered excited state lifetimes of Chl a. The observed energetic overlap of the fluorescence terminal energy emitters with the absorption of RCs is hypothesized to enable efficient downhill excitation energy transfer. Additionally, the shortened Chl a fluorescence decay lifetime in the oligomeric acpPC indicate a protective self-relaxation strategy. We propose that the highly-oligomerized acpPC nonamer represents an intact functional unit in the Symbiodiniaceae thylakoid membrane. They perform efficient excitation energy transfer (to RCs), and are under manageable regulations in favor of photoprotection.

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Acknowledgements

The authors thank Atsuko Kanazawa in David Kramer’s lab for sharing the Fugacium kawagutii strain and helpful discussion. D.N.M. acknowledges Center for Solar Energy and Energy Storage at McKelvey School of Engineering at Washington University in Saint Louis for finanacial support. N.C. M. M. was supported by the U.S. Department of Energy (DOE), Office of Basic Energy Sciences under grant DE-CD0002036 to Professors: Chris Kirmaier and Dewey Holten. This research was supported by the Danforth Seed Grant of Department of Biology at Washington University in Saint Louis (to H.L.). H. L. also acknowledges the U.S. Department of Energy (DOE), Office of Basic Energy Sciences, Photosynthetic Systems (PS) Program (Grant DE-FG02-07ER15902 to H.L.).

Funding

This study was supported by U.S. Department of Energy (Grant No. DE-FG02-07ER15902, DE-CD0002036), and Danforth Foundation, Seed grant Biology Washington University.

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Authors and Affiliations

  1. Center for Solar Energy and Energy Storage, Washington University in St. Louis, St. Louis, MO, 63130, USA

    Dariusz M. Niedzwiedzki

  2. Department of Energy Environmental and Chemical Engineering, Washington University in St. Louis, St. Louis, MO, 63130, USA

    Dariusz M. Niedzwiedzki

  3. Department of Chemistry, Washington University in St. Louis, St. Louis, MO, 63130, USA

    Nikki Cecil M. Magdaong

  4. Department of Biology, Washington University in St. Louis, St. Louis, MO, 63130, USA

    Xinyang Su & Haijun Liu

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  1. Dariusz M. Niedzwiedzki
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Correspondence to Dariusz M. Niedzwiedzki or Haijun Liu.

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Niedzwiedzki, D.M., Magdaong, N.C.M., Su, X. et al. Biochemical and spectroscopic characterizations of the oligomeric antenna of the coral symbiotic Symbiodiniaceae Fugacium kawagutii. Photosynth Res 154, 113–124 (2022). https://doi.org/10.1007/s11120-022-00951-6

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