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

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.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [5]; ORCiD logo [4]; ORCiD logo [3]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, Los Angeles, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  5. Univ. of California, San Francisco, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Brookhaven National Lab. (BNL), Upton, NY (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Brookhaven National Lab. (BNL), Upton, NY (United States); Univ. of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23). Biological Systems Science Division
OSTI Identifier:
1542375
Alternate Identifier(s):
OSTI ID: 1495514; OSTI ID: 1547018; OSTI ID: 1560877
Report Number(s):
BNL-211953-2019-JAAM
Journal ID: ISSN 1040-4651; ark:/13030/qt2js8161p
Grant/Contract Number:  
AC02-05CH11231; 2013-67012-21272; P41GM103445; 1S10OD018136-01; P01GM051487; SC0012704; SC0018301
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Plant Cell
Additional Journal Information:
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.
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. doi:10.1105/tpc.18.00742.
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. Tue . "Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis". United States. doi:10.1105/tpc.18.00742. https://www.osti.gov/servlets/purl/1542375.
@article{osti_1542375,
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 = {Plant Cell},
issn = {1040-4651},
number = 3,
volume = 31,
place = {United States},
year = {2019},
month = {4}
}

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