Structure of a PSI-LHCI-cyt b6f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions

Janina Steinbeck, Ian L. Ross, Rosalba Rothnagel, Philipp Gäbelein, Stefan Schulze, Nichole Giles, Rubbiya Ali, Rohan Drysdale, Emma Sierecki, Yann Gambin, Henning Stahlberg, Yuichiro Takahashi, Michael Hippler, Ben Hankamer

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11 Citations (Scopus)

Abstract

Photosynthetic linear electron flow (LEF) produces ATP and NADPH, while cyclic electron flow (CEF) exclusively drives photophosphorylation to supply extra ATP. The fine-tuning of linear and cyclic electron transport levels allows photosynthetic organisms to balance light energy absorption with cellular energy requirements under constantly changing light conditions. As LEF and CEF share many electron transfer components, a key question is how the same individual structural units contribute to these two different functional modes. Here, we report the structural identification of a photosystem I (PSI)-light harvesting complex I (LHCI)-cytochrome (cyt) b6f supercomplex isolated from the unicellular alga Chlamydomonas reinhardtii under anaerobic conditions, which induces CEF. This provides strong evidence for the model that enhanced CEF is induced by the formation of CEF supercomplexes, when stromal electron carriers are reduced, to generate additional ATP. The additional identification of PSI-LHCI- LHCII complexes is consistent with recent findings that both CEF enhancement and state transitions are triggered by similar conditions, but can occur independently from each other. Single molecule fluorescence correlation spectroscopy indicates a physical association between cyt b6f and fluorescent chlorophyll containing PSI-LHCI supercomplexes. Single particle analysis identified top-view projections of the corresponding PSI-LHCI-cyt b6f supercomplex. Based on molecular modeling and mass spectrometry analyses, we propose a model in which dissociation of LHCA2 and LHCA9 from PSI supports the formation of this CEF supercomplex. This is supported by the finding that a Δlhca2 knockout mutant has constitutively enhanced CEF.

Original languageEnglish
Pages (from-to)10517-10522
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number41
DOIs
Publication statusPublished - Oct 9 2018

Keywords

  • Chlamydomonas reinhardtii
  • Cyclic electron flow
  • Cytochrome bf
  • Photosystem I
  • Supercomplex

ASJC Scopus subject areas

  • General

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    Steinbeck, J., Ross, I. L., Rothnagel, R., Gäbelein, P., Schulze, S., Giles, N., Ali, R., Drysdale, R., Sierecki, E., Gambin, Y., Stahlberg, H., Takahashi, Y., Hippler, M., & Hankamer, B. (2018). Structure of a PSI-LHCI-cyt b6f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions. Proceedings of the National Academy of Sciences of the United States of America, 115(41), 10517-10522. https://doi.org/10.1073/pnas.1809973115