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Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum

Photoacclimation consists of short‐ and long‐term strategies used by photosynthetic organisms to adapt to dynamic light environments. Observable photophysiology changes resulting from these strategies have been used in coarse‐grained models to predict light‐dependent growth and photosynthetic rates....

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Autores principales: Broddrick, Jared T., Du, Niu, Smith, Sarah R., Tsuji, Yoshinori, Jallet, Denis, Ware, Maxwell A., Peers, Graham, Matsuda, Yusuke, Dupont, Chris L., Mitchell, B. Greg, Palsson, Bernhard O., Allen, Andrew E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6594073/
https://www.ncbi.nlm.nih.gov/pubmed/30636322
http://dx.doi.org/10.1111/nph.15685
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author Broddrick, Jared T.
Du, Niu
Smith, Sarah R.
Tsuji, Yoshinori
Jallet, Denis
Ware, Maxwell A.
Peers, Graham
Matsuda, Yusuke
Dupont, Chris L.
Mitchell, B. Greg
Palsson, Bernhard O.
Allen, Andrew E.
author_facet Broddrick, Jared T.
Du, Niu
Smith, Sarah R.
Tsuji, Yoshinori
Jallet, Denis
Ware, Maxwell A.
Peers, Graham
Matsuda, Yusuke
Dupont, Chris L.
Mitchell, B. Greg
Palsson, Bernhard O.
Allen, Andrew E.
author_sort Broddrick, Jared T.
collection PubMed
description Photoacclimation consists of short‐ and long‐term strategies used by photosynthetic organisms to adapt to dynamic light environments. Observable photophysiology changes resulting from these strategies have been used in coarse‐grained models to predict light‐dependent growth and photosynthetic rates. However, the contribution of the broader metabolic network, relevant to species‐specific strategies and fitness, is not accounted for in these simple models. We incorporated photophysiology experimental data with genome‐scale modeling to characterize organism‐level, light‐dependent metabolic changes in the model diatom Phaeodactylum tricornutum. Oxygen evolution and photon absorption rates were combined with condition‐specific biomass compositions to predict metabolic pathway usage for cells acclimated to four different light intensities. Photorespiration, an ornithine‐glutamine shunt, and branched‐chain amino acid metabolism were hypothesized as the primary intercompartment reductant shuttles for mediating excess light energy dissipation. Additionally, simulations suggested that carbon shunted through photorespiration is recycled back to the chloroplast as pyruvate, a mechanism distinct from known strategies in photosynthetic organisms. Our results suggest a flexible metabolic network in P. tricornutum that tunes intercompartment metabolism to optimize energy transport between the organelles, consuming excess energy as needed. Characterization of these intercompartment reductant shuttles broadens our understanding of energy partitioning strategies in this clade of ecologically important primary producers.
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spelling pubmed-65940732019-07-10 Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum Broddrick, Jared T. Du, Niu Smith, Sarah R. Tsuji, Yoshinori Jallet, Denis Ware, Maxwell A. Peers, Graham Matsuda, Yusuke Dupont, Chris L. Mitchell, B. Greg Palsson, Bernhard O. Allen, Andrew E. New Phytol Research Photoacclimation consists of short‐ and long‐term strategies used by photosynthetic organisms to adapt to dynamic light environments. Observable photophysiology changes resulting from these strategies have been used in coarse‐grained models to predict light‐dependent growth and photosynthetic rates. However, the contribution of the broader metabolic network, relevant to species‐specific strategies and fitness, is not accounted for in these simple models. We incorporated photophysiology experimental data with genome‐scale modeling to characterize organism‐level, light‐dependent metabolic changes in the model diatom Phaeodactylum tricornutum. Oxygen evolution and photon absorption rates were combined with condition‐specific biomass compositions to predict metabolic pathway usage for cells acclimated to four different light intensities. Photorespiration, an ornithine‐glutamine shunt, and branched‐chain amino acid metabolism were hypothesized as the primary intercompartment reductant shuttles for mediating excess light energy dissipation. Additionally, simulations suggested that carbon shunted through photorespiration is recycled back to the chloroplast as pyruvate, a mechanism distinct from known strategies in photosynthetic organisms. Our results suggest a flexible metabolic network in P. tricornutum that tunes intercompartment metabolism to optimize energy transport between the organelles, consuming excess energy as needed. Characterization of these intercompartment reductant shuttles broadens our understanding of energy partitioning strategies in this clade of ecologically important primary producers. John Wiley and Sons Inc. 2019-02-14 2019-05 /pmc/articles/PMC6594073/ /pubmed/30636322 http://dx.doi.org/10.1111/nph.15685 Text en © 2019 J. Craig Venter Institute New Phytologist © 2019 New Phytologist Trust This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Broddrick, Jared T.
Du, Niu
Smith, Sarah R.
Tsuji, Yoshinori
Jallet, Denis
Ware, Maxwell A.
Peers, Graham
Matsuda, Yusuke
Dupont, Chris L.
Mitchell, B. Greg
Palsson, Bernhard O.
Allen, Andrew E.
Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum
title Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum
title_full Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum
title_fullStr Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum
title_full_unstemmed Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum
title_short Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum
title_sort cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom phaeodactylum tricornutum
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6594073/
https://www.ncbi.nlm.nih.gov/pubmed/30636322
http://dx.doi.org/10.1111/nph.15685
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