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Title: Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism

Abstract

Photosynthetic microorganisms typically have multiple isoforms of the electron transfer protein ferredoxin, although we know little about their exact functions. Surprisingly, a Chlamydomonas reinhardtii mutant null for the ferredoxin-5 gene (FDX5) completely ceased growth in the dark, with both photosynthetic and respiratory functions severely compromised; growth in the light was unaffected. Thylakoid membranes in dark-maintained fdx5 mutant cells became severely disorganized concomitant with a marked decrease in the ratio of monogalactosyldiacylglycerol to digalactosyldiacylglycerol, major lipids in photosynthetic membranes, and the accumulation of triacylglycerol. Furthermore, FDX5 was shown to physically interact with the fatty acid desaturases CrΔ4FAD and CrFAD6, likely donating electrons for the desaturation of fatty acids that stabilize monogalactosyldiacylglycerol. Our results suggest that in photosynthetic organisms, specific redox reactions sustain dark metabolism, with little impact on daytime growth, likely reflecting the tailoring of electron carriers to unique intracellular metabolic circuits under these two very distinct redox conditions.

Authors:
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Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1337341
Alternate Identifier(s):
OSTI ID: 1235233
Report Number(s):
NREL/JA-2700-64784
Journal ID: ISSN 0027-8424; /pnas/112/48/14978.atom
Grant/Contract Number:  
AC36-08GO28308; FG02-07ER64427; FG02-12ER16338; FG02-12ER16339; IOS-1359682; GM42143; 1s10RR02678001
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 112 Journal Issue: 48; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Ferredoxin-5; chloroplast redox; thylakoid lipid composition; dark growth; triacylglycerol redox; regulation

Citation Formats

Yang, Wenqiang, Wittkopp, Tyler M., Li, Xiaobo, Warakanont, Jaruswan, Dubini, Alexandra, Catalanotti, Claudia, Kim, Rick G., Nowack, Eva C. M., Mackinder, Luke C. M., Aksoy, Munevver, Page, Mark Dudley, D’Adamo, Sarah, Saroussi, Shai, Heinnickel, Mark, Johnson, Xenie, Richaud, Pierre, Alric, Jean, Boehm, Marko, Jonikas, Martin C., Benning, Christoph, Merchant, Sabeeha S., Posewitz, Matthew C., and Grossman, Arthur R. Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism. United States: N. p., 2015. Web. doi:10.1073/pnas.1515240112.
Yang, Wenqiang, Wittkopp, Tyler M., Li, Xiaobo, Warakanont, Jaruswan, Dubini, Alexandra, Catalanotti, Claudia, Kim, Rick G., Nowack, Eva C. M., Mackinder, Luke C. M., Aksoy, Munevver, Page, Mark Dudley, D’Adamo, Sarah, Saroussi, Shai, Heinnickel, Mark, Johnson, Xenie, Richaud, Pierre, Alric, Jean, Boehm, Marko, Jonikas, Martin C., Benning, Christoph, Merchant, Sabeeha S., Posewitz, Matthew C., & Grossman, Arthur R. Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism. United States. doi:10.1073/pnas.1515240112.
Yang, Wenqiang, Wittkopp, Tyler M., Li, Xiaobo, Warakanont, Jaruswan, Dubini, Alexandra, Catalanotti, Claudia, Kim, Rick G., Nowack, Eva C. M., Mackinder, Luke C. M., Aksoy, Munevver, Page, Mark Dudley, D’Adamo, Sarah, Saroussi, Shai, Heinnickel, Mark, Johnson, Xenie, Richaud, Pierre, Alric, Jean, Boehm, Marko, Jonikas, Martin C., Benning, Christoph, Merchant, Sabeeha S., Posewitz, Matthew C., and Grossman, Arthur R. Mon . "Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism". United States. doi:10.1073/pnas.1515240112.
@article{osti_1337341,
title = {Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism},
author = {Yang, Wenqiang and Wittkopp, Tyler M. and Li, Xiaobo and Warakanont, Jaruswan and Dubini, Alexandra and Catalanotti, Claudia and Kim, Rick G. and Nowack, Eva C. M. and Mackinder, Luke C. M. and Aksoy, Munevver and Page, Mark Dudley and D’Adamo, Sarah and Saroussi, Shai and Heinnickel, Mark and Johnson, Xenie and Richaud, Pierre and Alric, Jean and Boehm, Marko and Jonikas, Martin C. and Benning, Christoph and Merchant, Sabeeha S. and Posewitz, Matthew C. and Grossman, Arthur R.},
abstractNote = {Photosynthetic microorganisms typically have multiple isoforms of the electron transfer protein ferredoxin, although we know little about their exact functions. Surprisingly, a Chlamydomonas reinhardtii mutant null for the ferredoxin-5 gene (FDX5) completely ceased growth in the dark, with both photosynthetic and respiratory functions severely compromised; growth in the light was unaffected. Thylakoid membranes in dark-maintained fdx5 mutant cells became severely disorganized concomitant with a marked decrease in the ratio of monogalactosyldiacylglycerol to digalactosyldiacylglycerol, major lipids in photosynthetic membranes, and the accumulation of triacylglycerol. Furthermore, FDX5 was shown to physically interact with the fatty acid desaturases CrΔ4FAD and CrFAD6, likely donating electrons for the desaturation of fatty acids that stabilize monogalactosyldiacylglycerol. Our results suggest that in photosynthetic organisms, specific redox reactions sustain dark metabolism, with little impact on daytime growth, likely reflecting the tailoring of electron carriers to unique intracellular metabolic circuits under these two very distinct redox conditions.},
doi = {10.1073/pnas.1515240112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 48,
volume = 112,
place = {United States},
year = {2015},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1073/pnas.1515240112

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Cited by: 7 works
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    Works referencing / citing this record:

    Discovery of CRR1-targeted copper deficiency response in Chlamydomonas reinhardtii exposed to silver nanoparticles
    journal, February 2019