skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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, should constitute anmore » excellent resource for the algal and plant communities.« less

Authors:
ORCiD logo; ; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ; ; ORCiD logo;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Lawrence Berkeley National Lab. (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; /pnas/116/6/2374.atom
Grant/Contract Number:  
FC02-02ER63421; AC05-76RL01830; AC02-05CH11231
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: 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: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. Fri . "Multiomics resolution of molecular events during a day in the life of Chlamydomonas". United States. doi: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 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},
number = 6,
volume = 116,
place = {United States},
year = {2019},
month = {1}
}

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

Citation Metrics:
Cited by: 12 works
Citation information provided by
Web of Science

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

Save / Share:

Works referenced in this record:

Anaerobic Acclimation in Chlamydomonas reinhardtii : ANOXIC GENE EXPRESSION, HYDROGENASE INDUCTION, AND METABOLIC PATHWAYS
journal, June 2007

  • Mus, Florence; Dubini, Alexandra; Seibert, Michael
  • Journal of Biological Chemistry, Vol. 282, Issue 35
  • DOI: 10.1074/jbc.M701415200

Arabidopsis Coordinates the Diurnal Regulation of Carbon Allocation and Growth across a Wide Range of Photoperiods
journal, January 2014

  • Sulpice, Ronan; Flis, Anna; Ivakov, Alexander A.
  • Molecular Plant, Vol. 7, Issue 1
  • DOI: 10.1093/mp/sst127

Analysis of light/dark synchronization of cell-wall-less Chlamydomonas reinhardtii (Chlorophyta) cells by flow cytometry
journal, August 1999

  • Lemaire, Stephane; Hours, Michel; Gerard-Hirne, Catherine
  • European Journal of Phycology, Vol. 34, Issue 3
  • DOI: 10.1080/09670269910001736332

Photosystem II Subunit PsbS Is Involved in the Induction of LHCSR Protein-dependent Energy Dissipation in Chlamydomonas reinhardtii
journal, June 2016

  • Correa-Galvis, Viviana; Redekop, Petra; Guan, Katharine
  • Journal of Biological Chemistry, Vol. 291, Issue 33
  • DOI: 10.1074/jbc.M116.737312

Histone H3 Dynamics in Plant Cell Cycle and Development
journal, January 2014

  • Otero, Sofía; Desvoyes, Bénédicte; Gutierrez, Crisanto
  • Cytogenetic and Genome Research, Vol. 143, Issue 1-3
  • DOI: 10.1159/000365264

Analysis of the Chloroplast Protein Kinase Stt7 during State Transitions
journal, March 2009


Clocks in Algae
journal, December 2014

  • Noordally, Zeenat B.; Millar, Andrew J.
  • Biochemistry, Vol. 54, Issue 2
  • DOI: 10.1021/bi501089x

Rationales and Approaches for Studying Metabolism in Eukaryotic Microalgae
journal, April 2014


Circadian Phase Has Profound Effects on Differential Expression Analysis
journal, November 2012


Pyruvate Formate-lyase and a Novel Route of Eukaryotic ATP Synthesis in Chlamydomonas Mitochondria
journal, February 2006

  • Atteia, Ariane; van Lis, Robert; Gelius-Dietrich, Gabriel
  • Journal of Biological Chemistry, Vol. 281, Issue 15
  • DOI: 10.1074/jbc.M507862200

The ATP Paradox Is the Expression of an Economizing Fuel Mechanism
journal, October 2004

  • Aledo, J. Carlos; del Valle, Alicia Esteban
  • Journal of Biological Chemistry, Vol. 279, Issue 53
  • DOI: 10.1074/jbc.M410479200

The organization structure and regulatory elements of Chlamydomonas histone genes reveal features linking plant and animal genes
journal, September 1995

  • Fabry, Stefan; M�ller, Kurt; Lindauer, Andreas
  • Current Genetics, Vol. 28, Issue 4
  • DOI: 10.1007/BF00326431

Identification of the Elusive Pyruvate Reductase of Chlamydomonas reinhardtii Chloroplasts
journal, November 2015

  • Burgess, Steven J.; Taha, Hussein; Yeoman, Justin A.
  • Plant and Cell Physiology, Vol. 57, Issue 1
  • DOI: 10.1093/pcp/pcv167

An ancient light-harvesting protein is critical for the regulation of algal photosynthesis
journal, November 2009

  • Peers, Graham; Truong, Thuy B.; Ostendorf, Elisabeth
  • Nature, Vol. 462, Issue 7272
  • DOI: 10.1038/nature08587

Proteomic analysis of a eukaryotic cilium
journal, July 2005

  • Pazour, Gregory J.; Agrin, Nathan; Leszyk, John
  • The Journal of Cell Biology, Vol. 170, Issue 1
  • DOI: 10.1083/jcb.200504008

Concerted Up-regulation of Aldehyde/Alcohol Dehydrogenase (ADHE) and Starch in Chlamydomonas reinhardtii Increases Survival under Dark Anoxia
journal, December 2016

  • van Lis, Robert; Popek, Marion; Couté, Yohann
  • Journal of Biological Chemistry, Vol. 292, Issue 6
  • DOI: 10.1074/jbc.M116.766048

Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012


Circadian control of carbohydrate availability for growth in Arabidopsis plants at night
journal, May 2010

  • Graf, A.; Schlereth, A.; Stitt, M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 20
  • DOI: 10.1073/pnas.0914299107

Ribonucleotide reductases and radical reactions
journal, July 1998


Functional Modeling Identifies Paralogous Solanesyl-diphosphate Synthases That Assemble the Side Chain of Plastoquinone-9 in Plastids
journal, August 2013

  • Block, Anna; Fristedt, Rikard; Rogers, Sara
  • Journal of Biological Chemistry, Vol. 288, Issue 38
  • DOI: 10.1074/jbc.M113.492769

Chlamydomonas as a model for biofuels and bio‐products production
journal, February 2015

  • Scranton, Melissa A.; Ostrand, Joseph T.; Fields, Francis J.
  • The Plant Journal, Vol. 82, Issue 3
  • DOI: 10.1111/tpj.12780

Light stress and photoprotection in Chlamydomonas reinhardtii
journal, March 2015

  • Erickson, Erika; Wakao, Setsuko; Niyogi, Krishna K.
  • The Plant Journal, Vol. 82, Issue 3
  • DOI: 10.1111/tpj.12825

Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light.
journal, June 2016

  • Tibiletti, Tania; Auroy, Pascaline; Peltier, Gilles
  • Plant Physiology
  • DOI: 10.1104/pp.16.00572

Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism
journal, April 2014

  • Schmollinger, Stefan; Mühlhaus, Timo; Boyle, Nanette R.
  • The Plant Cell, Vol. 26, Issue 4
  • DOI: 10.1105/tpc.113.122523

Quantitative analysis of the chemotaxis of a green alga, Chlamydomonas reinhardtii , to bicarbonate using diffusion-based microfluidic device
journal, January 2016

  • Choi, Hong Il; Kim, Jaoon Young Hwan; Kwak, Ho Seok
  • Biomicrofluidics, Vol. 10, Issue 1
  • DOI: 10.1063/1.4942756

MEN  /  nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles
journal, December 2008


Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism
journal, November 2015

  • Yang, Wenqiang; Wittkopp, Tyler M.; Li, Xiaobo
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 48
  • DOI: 10.1073/pnas.1515240112

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

Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail
journal, November 2008

  • Marzluff, William F.; Wagner, Eric J.; Duronio, Robert J.
  • Nature Reviews Genetics, Vol. 9, Issue 11
  • DOI: 10.1038/nrg2438

Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis
journal, January 2009

  • Piques, Maria; Schulze, Waltraud X.; Höhne, Melanie
  • Molecular Systems Biology, Vol. 5, Issue 1
  • DOI: 10.1038/msb.2009.68

Sugars and Circadian Regulation Make Major Contributions to the Global Regulation of Diurnal Gene Expression in Arabidopsis
journal, November 2005

  • Bläsing, Oliver E.; Gibon, Yves; Günther, Manuela
  • The Plant Cell, Vol. 17, Issue 12
  • DOI: 10.1105/tpc.105.035261

Organization and transcription of Volvox histone-encoding genes: similarities between algal and animal genes
journal, January 1990


Mitotic Replication of Deoxyribonucleic acid in Chlamydomonas Reinhardi
journal, January 1960

  • Sueoka, N.
  • Proceedings of the National Academy of Sciences, Vol. 46, Issue 1
  • DOI: 10.1073/pnas.46.1.83

Insights into the Evolution of Vitamin B12 Auxotrophy from Sequenced Algal Genomes
journal, May 2011

  • Helliwell, K. E.; Wheeler, G. L.; Leptos, K. C.
  • Molecular Biology and Evolution, Vol. 28, Issue 10
  • DOI: 10.1093/molbev/msr124

2016 update of the PRIDE database and its related tools
journal, November 2015

  • Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1145

Anaerobic energy metabolism in unicellular photosynthetic eukaryotes
journal, February 2013

  • Atteia, Ariane; van Lis, Robert; Tielens, Aloysius G. M.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
  • DOI: 10.1016/j.bbabio.2012.08.002

A Mutant in the ADH1 Gene of Chlamydomonas reinhardtii Elicits Metabolic Restructuring during Anaerobiosis
journal, January 2012

  • Magneschi, Leonardo; Catalanotti, Claudia; Subramanian, Venkataramanan
  • Plant Physiology, Vol. 158, Issue 3
  • DOI: 10.1104/pp.111.191569

Transcription Factor–Dependent Chromatin Remodeling at Heat Shock and Copper-Responsive Promoters in Chlamydomonas reinhardtii
journal, June 2011

  • Strenkert, Daniela; Schmollinger, Stefan; Sommer, Frederik
  • The Plant Cell, Vol. 23, Issue 6
  • DOI: 10.1105/tpc.111.085266

A bioactive peptide amidating enzyme is required for ciliogenesis
journal, May 2017

  • Kumar, Dhivya; Strenkert, Daniela; Patel-King, Ramila S.
  • eLife, Vol. 6
  • DOI: 10.7554/eLife.25728

Interactions Between Deoxyribonucleotide and DNA Synthesis
journal, June 1988


Hypoxic survival requires a 2-on-2 hemoglobin in a process involving nitric oxide
journal, June 2013

  • Hemschemeier, A.; Duner, M.; Casero, D.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 26
  • DOI: 10.1073/pnas.1302592110

3′ End Processing of a Long Nuclear-Retained Noncoding RNA Yields a tRNA-like Cytoplasmic RNA
journal, November 2008


Oscillating behavior of carbohydrate granule formation and dinitrogen fixation in the cyanobacterium Cyanothece sp. strain ATCC 51142.
journal, March 1994


Metabolite profiling for plant functional genomics
journal, November 2000

  • Fiehn, Oliver; Kopka, Joachim; Dörmann, Peter
  • Nature Biotechnology, Vol. 18, Issue 11
  • DOI: 10.1038/81137

A Spatial Interactome Reveals the Protein Organization of the Algal CO2-Concentrating Mechanism
journal, September 2017


Genetically Programmed Changes in Photosynthetic Cofactor Metabolism in Copper-deficient Chlamydomonas
journal, July 2016

  • Strenkert, Daniela; Limso, Clariss Ann; Fatihi, Abdelhak
  • Journal of Biological Chemistry, Vol. 291, Issue 36
  • DOI: 10.1074/jbc.M116.717413

Analysis of LhcSR3, a Protein Essential for Feedback De-Excitation in the Green Alga Chlamydomonas reinhardtii
journal, January 2011


COPPER RESPONSE REGULATOR1–Dependent and –Independent Responses of the Chlamydomonas reinhardtii Transcriptome to Dark Anoxia
journal, September 2013

  • Hemschemeier, Anja; Casero, David; Liu, Bensheng
  • The Plant Cell, Vol. 25, Issue 9
  • DOI: 10.1105/tpc.113.115741

Transcription of the nuclear and chloroplast genomes during the vegetative cell cycle in Chlamydomonas reinhardi
journal, March 1977


Incorporation of polypeptides into thylakoid membranes of Chlamydomonas reinhardtii. Cyclic variations
journal, May 1976


Cell cycle control by timer and sizer in Chlamydomonas
journal, August 1983

  • Donnan, Lorraine; John, Peter C. L.
  • Nature, Vol. 304, Issue 5927
  • DOI: 10.1038/304630a0

JTK_CYCLE: An Efficient Nonparametric Algorithm for Detecting Rhythmic Components in Genome-Scale Data Sets
journal, September 2010

  • Hughes, Michael E.; Hogenesch, John B.; Kornacker, Karl
  • Journal of Biological Rhythms, Vol. 25, Issue 5
  • DOI: 10.1177/0748730410379711

A Dual Strategy to Cope with High Light in Chlamydomonas reinhardtii
journal, February 2013

  • Allorent, Guillaume; Tokutsu, Ryutaro; Roach, Thomas
  • The Plant Cell, Vol. 25, Issue 2
  • DOI: 10.1105/tpc.112.108274

Evolution of Chlamydomonas reinhardtii ferredoxins and their interactions with [FeFe]-hydrogenases
journal, June 2017


A Microbial Avenue to Cell Cycle Control in the Plant Superkingdom
journal, October 2014


The roles of specific xanthophylls in photoprotection
journal, December 1997

  • Niyogi, K. K.; Bjorkman, O.; Grossman, A. R.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 25
  • DOI: 10.1073/pnas.94.25.14162

A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element
journal, December 2005

  • Kropat, J.; Tottey, S.; Birkenbihl, R. P.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 51
  • DOI: 10.1073/pnas.0507693102

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