A1 Refereed original research article in a scientific journal

Water oxidation by photosystem II is the primary source of electrons for sustained H2 photoproduction in nutrient-replete green algae




AuthorsSergey Kosourov, Valéria Nagy, Dmitry Shevela, Martina Jokel, Johannes Messinger, Yagut Allahverdiyeva

PublisherThe Academy

Publication year2020

JournalProceedings of the National Academy of Sciences of the United States of America

Journal name in sourceProceedings of the National Academy of Sciences of the United States of America

Journal acronymProc Natl Acad Sci U S A

Volume117

Issue47

First page 29629

Last page29636

Number of pages8

ISSN0027-8424

eISSN1091-6490

DOIhttps://doi.org/10.1073/pnas.2009210117

Self-archived copy’s web addresshttps://research.utu.fi/converis/portal/detail/Publication/50546273


Abstract
The unicellular green alga Chlamydomonas reinhardtii is capable of photosynthetic H2 production. H2 evolution occurs under anaerobic conditions and is difficult to sustain due to 1) competition between [FeFe]-hydrogenase (H2ase), the key enzyme responsible for H2 metabolism in algae, and the Calvin–Benson–Bassham (CBB) cycle for photosynthetic reductants and 2) inactivation of H2ase by O2 coevolved in photosynthesis. Recently, we achieved sustainable H2 photoproduction by shifting algae from continuous illumination to a train of short (1 s) light pulses, interrupted by longer (9 s) dark periods. This illumination regime prevents activation of the CBB cycle and redirects photosynthetic electrons to H2ase. Employing membrane-inlet mass spectrometry and H18O2, we now present clear evidence that efficient H2 photoproduction in pulse-illuminated algae depends primarily on direct water biophotolysis, where water oxidation at the donor side of photosystem II (PSII) provides electrons for the reduction of protons by H2ase downstream of photosystem I. This occurs exclusively in the absence of CO2 fixation, while with the activation of the CBB cycle by longer (8 s) light pulses the H2 photoproduction ceases and instead a slow overall H2 uptake is observed. We also demonstrate that the loss of PSII activity in DCMU-treated algae or in PSII-deficient mutant cells can be partly compensated for by the indirect (PSII-independent) H2 photoproduction pathway, but only for a short (<1 h) period. Thus, PSII activity is indispensable for a sustained process, where it is responsible for more than 92% of the final H2 yield.

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