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Title: Multiomics resolution of molecular events during a day in the life of Chlamydomonas

Abstract

The unicellular green algaChlamydomonas reinhardtiidisplays metabolic flexibility in response to a changing environment. We analyzed expression patterns of its three genomes in cells grown under light–dark cycles. Nearly 85% of transcribed genes show differential expression, with different sets of transcripts being up-regulated over the course of the day to coordinate cellular growth before undergoing cell division. Parallel measurements of select metabolites and pigments, physiological parameters, and a subset of proteins allow us to infer metabolic events and to evaluate the impact of the transcriptome on the proteome. Among the findings are the observations thatChlamydomonasexhibits lower respiratory activity at night compared with the day; multiple fermentation pathways, some oxygen-sensitive, are expressed at night in aerated cultures; we propose that the ferredoxin, FDX9, is potentially the electron donor to hydrogenases. The light stress-responsive genesPSBS,LHCSR1, andLHCSR3show an acute response to lights-on at dawn under abrupt dark-to-light transitions, whileLHCSR3genes also exhibit a later, second burst in expression in the middle of the day dependent on light intensity. Each response to light (acute and sustained) can be selectively activated under specific conditions. Our expression dataset, complemented with coexpression networks and metabolite profiling, should constitute an excellent resource for the algal and plant communities.

Authors:
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Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1491412
Alternate Identifier(s):
OSTI ID: 1501660; OSTI ID: 1561906
Report Number(s):
PNNL-SA-140230
Journal ID: ISSN 0027-8424
Grant/Contract Number:  
FC02-02ER63421; AC05-76RL01830; AC02-05CH11231
Resource Type:
Journal Article: 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: 116 Journal Issue: 6; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; photo-bioreactor; systems biology; cell division; histone expression; chloroplast

Citation Formats

Strenkert, Daniela, Schmollinger, Stefan, Gallaher, Sean D., Salomé, Patrice A., Purvine, Samuel O., Nicora, Carrie D., Mettler-Altmann, Tabea, Soubeyrand, Eric, Weber, Andreas P. M., Lipton, Mary S., Basset, Gilles J., and Merchant, Sabeeha S. Multiomics resolution of molecular events during a day in the life of Chlamydomonas. United States: N. p., 2019. Web. doi:10.1073/pnas.1815238116.
Strenkert, Daniela, Schmollinger, Stefan, Gallaher, Sean D., Salomé, Patrice A., Purvine, Samuel O., Nicora, Carrie D., Mettler-Altmann, Tabea, Soubeyrand, Eric, Weber, Andreas P. M., Lipton, Mary S., Basset, Gilles J., & Merchant, Sabeeha S. Multiomics resolution of molecular events during a day in the life of Chlamydomonas. United States. https://doi.org/10.1073/pnas.1815238116
Strenkert, Daniela, Schmollinger, Stefan, Gallaher, Sean D., Salomé, Patrice A., Purvine, Samuel O., Nicora, Carrie D., Mettler-Altmann, Tabea, Soubeyrand, Eric, Weber, Andreas P. M., Lipton, Mary S., Basset, Gilles J., and Merchant, Sabeeha S. 2019. "Multiomics resolution of molecular events during a day in the life of Chlamydomonas". United States. https://doi.org/10.1073/pnas.1815238116.
@article{osti_1491412,
title = {Multiomics resolution of molecular events during a day in the life of Chlamydomonas},
author = {Strenkert, Daniela and Schmollinger, Stefan and Gallaher, Sean D. and Salomé, Patrice A. and Purvine, Samuel O. and Nicora, Carrie D. and Mettler-Altmann, Tabea and Soubeyrand, Eric and Weber, Andreas P. M. and Lipton, Mary S. and Basset, Gilles J. and Merchant, Sabeeha S.},
abstractNote = {The unicellular green algaChlamydomonas reinhardtiidisplays metabolic flexibility in response to a changing environment. We analyzed expression patterns of its three genomes in cells grown under light–dark cycles. Nearly 85% of transcribed genes show differential expression, with different sets of transcripts being up-regulated over the course of the day to coordinate cellular growth before undergoing cell division. Parallel measurements of select metabolites and pigments, physiological parameters, and a subset of proteins allow us to infer metabolic events and to evaluate the impact of the transcriptome on the proteome. Among the findings are the observations thatChlamydomonasexhibits lower respiratory activity at night compared with the day; multiple fermentation pathways, some oxygen-sensitive, are expressed at night in aerated cultures; we propose that the ferredoxin, FDX9, is potentially the electron donor to hydrogenases. The light stress-responsive genesPSBS,LHCSR1, andLHCSR3show an acute response to lights-on at dawn under abrupt dark-to-light transitions, whileLHCSR3genes also exhibit a later, second burst in expression in the middle of the day dependent on light intensity. Each response to light (acute and sustained) can be selectively activated under specific conditions. Our expression dataset, complemented with coexpression networks and metabolite profiling, should constitute an excellent resource for the algal and plant communities.},
doi = {10.1073/pnas.1815238116},
url = {https://www.osti.gov/biblio/1491412}, journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 6,
volume = 116,
place = {United States},
year = {Fri Jan 18 00:00:00 EST 2019},
month = {Fri Jan 18 00:00:00 EST 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.1073/pnas.1815238116

Citation Metrics:
Cited by: 68 works
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Figures / Tables:

Figure 1 Figure 1: How to obtain exactly two daughter cells during the Chlamydomonas cell division cycle. (A) Schematic illustration of the flat-panel photobioreactor design. (B–F) Experimental parameters measured under our growth conditions. Real-time profiles of the growth medium temperature (B), pH (C), and optical density at 680 nm (D). (E) Distributionmore » of cell size over the diurnal cycle, shown as a box plot. (F) Number of cells in the culture as a function of diurnal time. Data (except E) are shown as average ± SD (n = 3–9, specified in each panel). The green triangles indicate the timing of cell division.« less

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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.