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

Authors :
Yusuke Matsuda
Maxwell A. Ware
Graham Peers
Yoshinori Tsuji
Jared T. Broddrick
Denis Jallet
Andrew E. Allen
Christopher L. Dupont
Bernhard O. Palsson
B. Greg Mitchell
Niu Du
Sarah R. Smith
Système membranaires, photobiologie, stress et détoxication (SMPSD)
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)
Department of Biology [Fort Collins]
Colorado State University [Fort Collins] (CSU)
Infection et inflammation (2I)
Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Institut National de la Santé et de la Recherche Médicale (INSERM)
Scripps Institution of Oceanography (SIO)
University of California [San Diego] (UC San Diego)
University of California-University of California
Department of Bioengineering
Scripps Institution of Oceanography (SIO - UC San Diego)
University of California (UC)-University of California (UC)
Source :
The New Phytologist, New Phytologist, New Phytologist, Wiley, 2019, 222 (3), pp.1364-1379. ⟨10.1111/nph.15685⟩, New Phytologist, 2019, 222 (3), pp.1364-1379. ⟨10.1111/nph.15685⟩
Publication Year :
2019
Publisher :
Wiley, 2019.

Abstract

International audience; 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 intercompart-ment 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.

Details

ISSN :
14698137 and 0028646X
Volume :
222
Database :
OpenAIRE
Journal :
New Phytologist
Accession number :
edsair.doi.dedup.....2037ce5eff1398daf8ce5ff102f47a5e
Full Text :
https://doi.org/10.1111/nph.15685