Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis

Roth, Melissa S.; Gallaher, Sean D.; Westcott, Daniel J.; Iwai, Masakazu; Louie, Katherine B.; Mueller, Maria; Walter, Andreas; Foflonker, Fatima; Bowen, Benjamin P.; Ataii, Nassim N.; Song, Junha; Chen, Jian-Hua; Blaby-Haas, Crysten E.; Larabell, Carolyn; Auer, Manfred; Northen, Trent R.; Merchant, Sabeeha S.; Niyogi, Krishna K.

doi:10.1105/tpc.18.00742

Title: Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis

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Abstract

Light and nutrients are critical regulators of photosynthesis and metabolism in plants and algae. Many algae have the metabolic flexibility to grow photoautotrophically, heterotrophically, or mixotrophically. Here, we describe reversible glucose-dependent repression/activation of oxygenic photosynthesis in the unicellular green alga Chromochloris zofingiensis. We observed rapid and reversible changes in photosynthesis, in the photosynthetic apparatus, in thylakoid ultrastructure, and in energy stores including lipids and starch. Following glucose addition in the light, C. zofingiensis shuts off photosynthesis within days and accumulates large amounts of commercially relevant bioproducts, including triacylglycerols (TAGs) and the high-value nutraceutical ketocarotenoid astaxanthin, while increasing culture biomass. RNA sequencing reveals reversible changes in the transcriptome that form the basis of this metabolic regulation. Functional enrichment analyses show that glucose represses photosynthetic pathways while ketocarotenoid biosynthesis and heterotrophic carbon metabolism are upregulated. Because sugars play fundamental regulatory roles in gene expression, physiology, metabolism, and growth in both plants and animals, we have developed a simple algal model system to investigate conserved eukaryotic sugar responses as well as mechanisms of thylakoid breakdown and biogenesis in chloroplasts. Understanding regulation of photosynthesis and metabolism in algae could enable bioengineering to reroute metabolism toward beneficial bioproducts for energy, food, pharmaceuticals, and human health.

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Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102; Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720
Department of Chemistry and Biochemistry and Institute for Genomics and Proteomics, University of California, Los Angeles, California 90095-1569
Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720; U.S. Department of Energy Joint Genome Institute, Walnut Creek, California 94598
Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720; Joint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, California 94720
Department of Anatomy, University of California, San Francisco, California 94143; National Center for X-ray Tomography, Lawrence Berkeley National Laboratory, Berkeley, California 94720
Biology Department, Brookhaven National Laboratory, Upton, New York 11973
Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720

Publication Date:: Wed Feb 20 00:00:00 EST 2019

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States); University of California, Berkeley, CA (United States)

Sponsoring Org.:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

OSTI Identifier:: 1495514

Alternate Identifier(s):: OSTI ID: 1542375; OSTI ID: 1547018; OSTI ID: 1560877

Report Number(s):: BNL-211953-2019-JAAM
Journal ID: ISSN 1040-4651; /plantcell/31/3/579.atom

Grant/Contract Number:: 2013-67012-21272; AC02-05CH11231; P41GM103445; 1S10OD018136-01; P01GM051487; SC0012704; SC0018301

Resource Type:: Published Article

Journal Name:: The Plant Cell

Additional Journal Information:: Journal Name: The Plant Cell Journal Volume: 31 Journal Issue: 3; Journal ID: ISSN 1040-4651

Publisher:: American Society of Plant Biologists

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Roth, Melissa S., Gallaher, Sean D., Westcott, Daniel J., Iwai, Masakazu, Louie, Katherine B., Mueller, Maria, Walter, Andreas, Foflonker, Fatima, Bowen, Benjamin P., Ataii, Nassim N., Song, Junha, Chen, Jian-Hua, Blaby-Haas, Crysten E., Larabell, Carolyn, Auer, Manfred, Northen, Trent R., Merchant, Sabeeha S., and Niyogi, Krishna K. Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis.  United States: N. p., 2019. 
Web.  doi:10.1105/tpc.18.00742.

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                    Roth, Melissa S., Gallaher, Sean D., Westcott, Daniel J., Iwai, Masakazu, Louie, Katherine B., Mueller, Maria, Walter, Andreas, Foflonker, Fatima, Bowen, Benjamin P., Ataii, Nassim N., Song, Junha, Chen, Jian-Hua, Blaby-Haas, Crysten E., Larabell, Carolyn, Auer, Manfred, Northen, Trent R., Merchant, Sabeeha S., & Niyogi, Krishna K. Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis.  United States.  https://doi.org/10.1105/tpc.18.00742

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                    Roth, Melissa S., Gallaher, Sean D., Westcott, Daniel J., Iwai, Masakazu, Louie, Katherine B., Mueller, Maria, Walter, Andreas, Foflonker, Fatima, Bowen, Benjamin P., Ataii, Nassim N., Song, Junha, Chen, Jian-Hua, Blaby-Haas, Crysten E., Larabell, Carolyn, Auer, Manfred, Northen, Trent R., Merchant, Sabeeha S., and Niyogi, Krishna K. Wed .  
"Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis".  United States.  https://doi.org/10.1105/tpc.18.00742.

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@article{osti_1495514,

  title        = {Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis},

  author       = {Roth, Melissa S. and Gallaher, Sean D. and Westcott, Daniel J. and Iwai, Masakazu and Louie, Katherine B. and Mueller, Maria and Walter, Andreas and Foflonker, Fatima and Bowen, Benjamin P. and Ataii, Nassim N. and Song, Junha and Chen, Jian-Hua and Blaby-Haas, Crysten E. and Larabell, Carolyn and Auer, Manfred and Northen, Trent R. and Merchant, Sabeeha S. and Niyogi, Krishna K.},

  abstractNote = {Light and nutrients are critical regulators of photosynthesis and metabolism in plants and algae. Many algae have the metabolic flexibility to grow photoautotrophically, heterotrophically, or mixotrophically. Here, we describe reversible glucose-dependent repression/activation of oxygenic photosynthesis in the unicellular green alga Chromochloris zofingiensis. We observed rapid and reversible changes in photosynthesis, in the photosynthetic apparatus, in thylakoid ultrastructure, and in energy stores including lipids and starch. Following glucose addition in the light, C. zofingiensis shuts off photosynthesis within days and accumulates large amounts of commercially relevant bioproducts, including triacylglycerols (TAGs) and the high-value nutraceutical ketocarotenoid astaxanthin, while increasing culture biomass. RNA sequencing reveals reversible changes in the transcriptome that form the basis of this metabolic regulation. Functional enrichment analyses show that glucose represses photosynthetic pathways while ketocarotenoid biosynthesis and heterotrophic carbon metabolism are upregulated. Because sugars play fundamental regulatory roles in gene expression, physiology, metabolism, and growth in both plants and animals, we have developed a simple algal model system to investigate conserved eukaryotic sugar responses as well as mechanisms of thylakoid breakdown and biogenesis in chloroplasts. Understanding regulation of photosynthesis and metabolism in algae could enable bioengineering to reroute metabolism toward beneficial bioproducts for energy, food, pharmaceuticals, and human health.},

  doi          = {10.1105/tpc.18.00742},

  journal      = {The Plant Cell},

  number       = 3,

  volume       = 31,

  place        = {United States},

  year         = {Wed Feb 20 00:00:00 EST 2019},

  month        = {Wed Feb 20 00:00:00 EST 2019}

}

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