Iron rescues glucose-mediated photosynthesis repression during lipid accumulation in the green alga Chromochloris zofingiensis

Jeffers, Tim L.; Purvine, Samuel O.; Nicora, Carrie D.; McCombs, Ryan; Upadhyaya, Shivani; Stroumza, Adrien; Whang, Ken; Gallaher, Sean D.; Dohnalkova, Alice; Merchant, Sabeeha S.; Lipton, Mary S.; Niyogi, Krishna K.; Roth, Melissa S.

doi:10.1038/s41467-024-50170-x

Iron rescues glucose-mediated photosynthesis repression during lipid accumulation in the green alga Chromochloris zofingiensis

Journal Article · Thu Jul 18 00:00:00 EDT 2024 · Nature Communications

DOI:https://doi.org/10.1038/s41467-024-50170-x· OSTI ID:2439406

Jeffers, Tim L. ^[1]; ^[2]; ^[3]; ^[1]; ^[1]; Stroumza, Adrien ^[1]; Whang, Ken ^[1]; ^[4]; ^[2]; ^[5]; ^[2]; ^[5]; ^[1]

University of California, Berkeley, CA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Univ. of California, Los Angeles, CA (United States). UCLA-DOE Institute for Genomics and Proteomics (IGP); University of California, Berkeley, CA (United States)
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Energy status and nutrients regulate photosynthetic protein expression. The unicellular green alga Chromochloris zofingiensis switches off photosynthesis in the presence of exogenous glucose (+Glc) in a process that depends on hexokinase (HXK1). Here, we show that this response requires that cells lack sufficient iron (–Fe). Cells grown in –Fe+Glc accumulate triacylglycerol (TAG) while losing photosynthesis and thylakoid membranes. However, cells with an iron supplement (+Fe+Glc) maintain photosynthesis and thylakoids while still accumulating TAG. Proteomic analysis shows that known photosynthetic proteins are most depleted in heterotrophy, alongside hundreds of uncharacterized, conserved proteins. Photosynthesis repression is associated with enzyme and transporter regulation that redirects iron resources to (a) respiratory instead of photosynthetic complexes and (b) a ferredoxin-dependent desaturase pathway supporting TAG accumulation rather than thylakoid lipid synthesis. Combining insights from diverse organisms from green algae to vascular plants, we show how iron and trophic constraints on metabolism aid gene discovery for photosynthesis and biofuel production.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; SC0018301

OSTI ID:: 2439406

Alternate ID(s):: OSTI ID: 2440633

Report Number(s):: PNNL-SA--188046

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Chromochloris zofingiensis
biofuels
iron homeostasis
lipid accumulation
photosynthesis
plant evolution
plant stress responses

Iron rescues glucose-mediated photosynthesis repression during lipid accumulation in the green alga Chromochloris zofingiensis

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