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

Journal Article · · New Phytologist
DOI: https://doi.org/10.1111/nph.15685 · OSTI ID:1498802
 [1];  [2];  [3];  [4];  [5];  [5];  [5];  [4];  [3];  [6];  [7];  [2]
  1. Division of Biological Sciences UC San Diego La Jolla CA 92093 USA, Department of Bioengineering UC San Diego La Jolla CA 92093 USA
  2. Scripps Institution of Oceanography UC San Diego La Jolla CA 92093 USA, J. Craig Venter Institute La Jolla CA 92037 USA
  3. J. Craig Venter Institute La Jolla CA 92037 USA
  4. Department of Environmental Bioscience Kwansei Gakuin University Sanda 669‐1337 Japan
  5. Department of Biology Colorado State University Fort Collins CO 80523 USA
  6. Scripps Institution of Oceanography UC San Diego La Jolla CA 92093 USA
  7. Department of Bioengineering UC San Diego La Jolla CA 92093 USA
+ Show Author Affiliations

Summary 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.

Research Organization:
Colorado State University, Fort Collins, CO (United States); J. Craig Venter Institute, Inc., Rockville, MD (United States); University of California, San Diego, CA (United States)
Sponsoring Organization:
Gordon and Betty Moore Foundation (GBMF); Japan Society for the Promotion of Science (JSPS) KAKENHI; National Science Foundation (NSF); USDOE; USDOE Office of Energy Efficiency and Renewable Energy (EERE); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
EE0003373; SC0008593; SC0008595; SC0008701
OSTI ID:
1498802
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 3 Vol. 222; ISSN 0028-646X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

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59 BASIC BIOLOGICAL SCIENCES
Phaeodactylum tricornutum
analysis
diatom
energy metabolism
flux balance
genome-scale modeling
photorespiration
plant sciences