Photosystem II-cyclic electron flow powers exceptional photoprotection and record growth in the microalga Chlorella ohadii

Gennady Ananyev, Colin Gates, Aaron Kaplan, G. Charles Dismukes

Research output: Contribution to journalArticlepeer-review

11 Citations (Scopus)

Abstract

The desert microalga Chlorella ohadii was reported to grow at extreme light intensities with minimal photoinhibition, tolerate frequent de/re-hydrations, yet minimally employs antenna-based non-photochemical quenching for photoprotection. Here we investigate the molecular mechanisms by measuring Photosystem II charge separation yield (chlorophyll variable fluorescence, Fv/Fm) and flash-induced O 2 yield to measure the contributions from both linear (PSII-LEF) and cyclic (PSII-CEF) electron flow within PSII. Cells grow increasingly faster at higher light intensities (μE/m 2 /s) from low (20) to high (200) to extreme (2000) by escalating photoprotection via shifting from PSII-LEF to PSII-CEF. This shifts PSII charge separation from plastoquinone reduction (PSII-LEF) to plastoquinol oxidation (PSII-CEF), here postulated to enable proton gradient and ATP generation that powers photoprotection. Low light-grown cells have unusually small antennae (332 Chl/PSII), use mainly PSII-LEF (95%) and convert 40% of PSII charge separations into O 2 (a high O 2 quantum yield of 0.06 mol/mol PSII/flash). High light-grown cells have smaller antenna and lower PSII-LEF (63%). Extreme light-grown cells have only 42 Chl/PSII (no LHCII antenna), minimal PSII-LEF (10%), and grow faster than any known phototroph (doubling time 1.3 h). Adding a synthetic quinone in excess to supplement the PQ pool fully uncouples PSII-CEF from its natural regulation and produces maximum PSII-LEF. Upon dark adaptation PSII-LEF rapidly reverts to PSII-CEF, a transient protection mechanism to conserve water and minimize the cost of antenna biosynthesis. The capacity of the electron acceptor pool (plastoquinone pool), and the characteristic times for exchange of (PQH 2 ) B with PQ pool and reoxidation of (PQH 2 ) pool were determined.

Original languageEnglish
Pages (from-to)873-883
Number of pages11
JournalBiochimica et Biophysica Acta - Bioenergetics
Volume1858
Issue number11
DOIs
Publication statusPublished - Nov 2017

Keywords

  • Chlorella ohadii
  • Cyclic electron transfer
  • Oxygen evolution
  • Photosynthetic efficiency
  • VZAD model
  • Water oxidation

ASJC Scopus subject areas

  • Biophysics
  • Biochemistry
  • Cell Biology

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