Depletion reveals role of bicarbonate in the photosynthetic electron transport chain of Limnospira maxima

Efficient photosynthetic light reactions require tight balancing of electrons and protons. In photosystem II, bicarbonate is coordinated to a non-heme iron positioned between the acceptor-side plastoquinones QA and QB, modulating electron transfer. The hypercarbonate-requiring filamentous cyanobacte...

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Main Authors: Leslie Castillo, Stavroula Nicolaou, Colin Gates
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-06-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1584909/full
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author Leslie Castillo
Stavroula Nicolaou
Colin Gates
Colin Gates
author_facet Leslie Castillo
Stavroula Nicolaou
Colin Gates
Colin Gates
author_sort Leslie Castillo
collection DOAJ
description Efficient photosynthetic light reactions require tight balancing of electrons and protons. In photosystem II, bicarbonate is coordinated to a non-heme iron positioned between the acceptor-side plastoquinones QA and QB, modulating electron transfer. The hypercarbonate-requiring filamentous cyanobacterium Limnospira maxima has had multiple bicarbonate functions on both acceptor and donor side of PSII determined by depletion. 77K spectrofluorometric investigation of phycobilin and chlorophyll excitation suggests the mild in vivo depletion method for bicarbonate results in loss of chlorophyll connectivity to the reaction center in PSII and dissociation of the phycobilisome due to proportional increase of fluorescence emission from allophycocyanin. Using chlorophyll fast repetition rate fluorometry, it was observed under bicarbonate depletion that oscillations were still present in a fraction of PSIIs, confirming the functionality of the water oxidizing complex remains in this fraction of centers. In these fractions of centers only one to two electrons are being released. QA- reoxidation kinetics indicate that loss of bicarbonate permits successful electron transfer to QB, forming semiquinone QB-. DCMU inhibition of the second electron transfer implies that, in bicarbonate-depleted L. maxima, electron transfer to QB affects proton delivery needed for plastoquinol formation, which suggests that this depletion targets the non-heme iron. Based on cytochrome b6f redox kinetics, depleted cells experience less intensity of oxidation and upon illumination cytochrome b and f are proportionally rapidly and intensely oxidized. P700 redox kinetics exhibit a delay feature in PSI as well as the expected delay of electron delivery to PSII, suggesting a further bicarbonate effect on PSI.
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spelling doaj-art-57e61757dab8472bb9269e576c5f80ef2025-08-20T02:39:52ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-06-011610.3389/fpls.2025.15849091584909Depletion reveals role of bicarbonate in the photosynthetic electron transport chain of Limnospira maximaLeslie Castillo0Stavroula Nicolaou1Colin Gates2Colin Gates3Department of Chemistry and Biochemistry, Loyola University Chicago, Chicago, IL, United StatesDepartment of Biology, Loyola University Chicago, Chicago, IL, United StatesDepartment of Chemistry and Biochemistry, Loyola University Chicago, Chicago, IL, United StatesDepartment of Bioinformatics, Loyola University Chicago, Chicago, IL, United StatesEfficient photosynthetic light reactions require tight balancing of electrons and protons. In photosystem II, bicarbonate is coordinated to a non-heme iron positioned between the acceptor-side plastoquinones QA and QB, modulating electron transfer. The hypercarbonate-requiring filamentous cyanobacterium Limnospira maxima has had multiple bicarbonate functions on both acceptor and donor side of PSII determined by depletion. 77K spectrofluorometric investigation of phycobilin and chlorophyll excitation suggests the mild in vivo depletion method for bicarbonate results in loss of chlorophyll connectivity to the reaction center in PSII and dissociation of the phycobilisome due to proportional increase of fluorescence emission from allophycocyanin. Using chlorophyll fast repetition rate fluorometry, it was observed under bicarbonate depletion that oscillations were still present in a fraction of PSIIs, confirming the functionality of the water oxidizing complex remains in this fraction of centers. In these fractions of centers only one to two electrons are being released. QA- reoxidation kinetics indicate that loss of bicarbonate permits successful electron transfer to QB, forming semiquinone QB-. DCMU inhibition of the second electron transfer implies that, in bicarbonate-depleted L. maxima, electron transfer to QB affects proton delivery needed for plastoquinol formation, which suggests that this depletion targets the non-heme iron. Based on cytochrome b6f redox kinetics, depleted cells experience less intensity of oxidation and upon illumination cytochrome b and f are proportionally rapidly and intensely oxidized. P700 redox kinetics exhibit a delay feature in PSI as well as the expected delay of electron delivery to PSII, suggesting a further bicarbonate effect on PSI.https://www.frontiersin.org/articles/10.3389/fpls.2025.1584909/fullphotosystem IIbicarbonatenon-heme ironplastoquinonephotosynthetic electron transport chainarthrospira maxima
spellingShingle Leslie Castillo
Stavroula Nicolaou
Colin Gates
Colin Gates
Depletion reveals role of bicarbonate in the photosynthetic electron transport chain of Limnospira maxima
Frontiers in Plant Science
photosystem II
bicarbonate
non-heme iron
plastoquinone
photosynthetic electron transport chain
arthrospira maxima
title Depletion reveals role of bicarbonate in the photosynthetic electron transport chain of Limnospira maxima
title_full Depletion reveals role of bicarbonate in the photosynthetic electron transport chain of Limnospira maxima
title_fullStr Depletion reveals role of bicarbonate in the photosynthetic electron transport chain of Limnospira maxima
title_full_unstemmed Depletion reveals role of bicarbonate in the photosynthetic electron transport chain of Limnospira maxima
title_short Depletion reveals role of bicarbonate in the photosynthetic electron transport chain of Limnospira maxima
title_sort depletion reveals role of bicarbonate in the photosynthetic electron transport chain of limnospira maxima
topic photosystem II
bicarbonate
non-heme iron
plastoquinone
photosynthetic electron transport chain
arthrospira maxima
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1584909/full
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AT colingates depletionrevealsroleofbicarbonateinthephotosyntheticelectrontransportchainoflimnospiramaxima
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