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

Abstract

The unicellular green alga Chlamydomonas reinhardtii displays 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 that Chlamydomonas exhibits 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 genes PSBS , LHCSR1 , and LHCSR3 show an acute response to lights-on at dawn under abrupt dark-to-light transitions, while LHCSR3 genes 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, shouldmore » constitute an excellent resource for the algal and plant communities.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4];  [3];  [2]; ORCiD logo [4];  [1]
  1. Univ. of California, Los Angeles, CA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Heinrich Heine University, Düsseldorf (Germany)
  4. Univ. of Nebraska, Lincoln, NE (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1501660
Alternate Identifier(s):
OSTI ID: 1491412
Report Number(s):
PNNL-SA-140230
Journal ID: ISSN 0027-8424
Grant/Contract Number:  
AC05-76RL01830; FC02-02ER63421
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
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. 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., and Merchant, Sabeeha S. Tue . "Multiomics resolution of molecular events during a day in the life of Chlamydomonas". United States. doi:10.1073/pnas.1815238116. https://www.osti.gov/servlets/purl/1501660.
@article{osti_1501660,
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 alga Chlamydomonas reinhardtii displays 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 that Chlamydomonas exhibits 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 genes PSBS , LHCSR1 , and LHCSR3 show an acute response to lights-on at dawn under abrupt dark-to-light transitions, while LHCSR3 genes 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},
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 = {2019},
month = {2}
}

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Works referenced in this record:

The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions
journal, October 2007

  • Merchant, S. S.; Prochnik, S. E.; Vallon, O.
  • Science, Vol. 318, Issue 5848, p. 245-250
  • DOI: 10.1126/science.1143609