Metabolic, physiological, and transcriptomics analysis of batch cultures of the green microalga Chlamydomonas grown on different acetate concentrations
Radoux, Michèle ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Eppe, Gauthier ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie analytique inorganique
Levine, Raphaël David
Remacle, Françoise ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de chimie physique théorique
Remacle, Claire ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Language :
English
Title :
Metabolic, physiological, and transcriptomics analysis of batch cultures of the green microalga Chlamydomonas grown on different acetate concentrations
Publication date :
2019
Journal title :
Cells
eISSN :
2073-4409
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Basel, Switzerland
Volume :
8
Pages :
367
Peer reviewed :
Peer Reviewed verified by ORBi
European Projects :
FP7 - 618024 - BAMBI - Bottom-up Approaches to Machines dedicated to Bayesian Inference
Fan, J.; Yan, C.; Andre, C.; Shanklin, J.; Schwender, J.; Xu, C. Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol. 2012, 53, 1380– 1390.
Plancke, C.; Vigeolas, H.; Höhner, R.; Roberty, S.; Emonds-Alt, B.; Larosa, V.; Willamme, R.; Duby, F.; Onga Dhali, D.; Thonart, P.; et al. Lack of isocitrate lyase in Chlamydomonas leads to changes in carbon metabolism and in the response to oxidative stress under mixotrophic growth. Plant J. 2014, 77, 404–417.
Salinas, T.; Larosa, V.; Cardol, P.; Maréchal-Drouard, L.; Remacle, C. Respiratory-deficient mutants of the unicellular green alga Chlamydomonas: A review. Biochimie 2014, 100, 207–218.
Harris, E.H. The Chlamydomonas Sourcebook; Elsevier Inc.: Amsterdam, The Netherlands, 1989; p. 26.
Heifetz, P.B.; Förster, B.; Osmond, C.B.; Giles, L.J.; Boynton, J.E. Effects of acetate on facultative autotrophy in Chlamydomonas reinhardtii assessed by photosynthetic measurements and stable isotope analyses. Plant Physiol. 2000, 122, 1439–1445.
Humby, P.L.; Snyder, E.C.R.; Durnford, D.G. Conditional senescence in Chlamydomonas reinhardtii (Chlorophyceae). J. Phycol. 2013, 49, 389–400.
Martinez, M.J. Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: Gene expression and identification of novel essential genes. Mol. Biol. Cell 2004, 15, 5295–5305.
Kamei, Y.; Tamada, Y.; Nakayama, Y.; Fukusaki, E.; Mukai, Y. Changes in transcription and metabolism during the early stage of replicative cellular senescence in budding yeast. J. Biol. Chem. 2014, 289, 32081– 32093.
Pérez-Pérez, M.E.; Crespo, J.L. Autophagy in the model alga Chlamydomonas reinhardtii. Autophagy 2010, 6, 562–563.
Esperanza, M.; Houde, M.; Seoane, M.; Cid, Á.; Rioboo, C. Does a short-term exposure to atrazine provoke cellular senescence in Chlamydomonas reinhardtii? Aquat. Toxicol. 2017, 189, 184–193.
Bogaert, K.A.; Manoharan-Basil, S.S.; Perez, E.; Levine, R.D.; Remacle, F.; Remacle, C. Surprisal analysis of genome-wide transcript profiling identifies differentially expressed genes and pathways associated with four growth conditions in the microalga Chlamydomonas. PLoS ONE 2018, 13, e0195142.
Remacle, F.; Kravchenko-Balasha, N.; Levitzki, A.; Levine, R.D. Information-theoretic analysis of phenotype changes in early stages of carcinogenesis. Proc. Natl. Acad. Sci. USA 2010, 107, 10324–10329.
Remacle, F.; Levine, R.D. Statistical thermodynamics of transcription profiles in normal development and tumorigeneses in cohorts of patients. Eur. Biophys. J. 2015, 44, 709–726.
Kravchenko-Balasha, N.; Remacle, F.; Gross, A.; Rotter, V.; Levitzki, A.; Levine, R.D. Convergence of logic of cellular regulation in different premalignant cells by an information theoretic approach. BMC Syst. Biol. 2011, 5, 42.
Kravchenko-Balasha, N.; Levitzki, A.; Goldstein, A.; Rotter, V.; Gross, A.; Remacle, F.; Levine, R.D. On a fundamental structure of gene networks in living cells. Proc. Natl. Acad. Sci. USA 2012, 109, 4702–4707.
Zadran, S.; Remacle, F.; Levine, R.D. miRNA and mRNA cancer signatures determined by analysis of expression levels in large cohorts of patients. Proc. Natl. Acad. Sci. USA 2013, 110, 19160–19165.
Fakhimi, N.; Dubini, A.; Tavakoli, O.; González-Ballester, D. Acetic acid is key for synergetic hydrogen production in Chlamydomonas-bacteria co-cultures. Bioresour. Technol. 2019, 289, 121648.
Willamme, R.; Alsafra, Z.; Arumugam, R.; Eppe, G.; Remacle, F.; Levine, R.D.D.; Remacle, C. Metabolomic analysis of the green microalga Chlamydomonas reinhardtii cultivated under day/night conditions. J. Biotechnol. 2015, 215, 20–26.
Pröschold, T.; Harris, E.H.; Coleman, A.W. Portrait of a species: Chlamydomonas reinhardtii. Genetics 2005, 170, 1601–1610.
Pulich, W.M.; Ward, C.H. Physiology and ultrastructure of an oxygen-resistant Chlorella mutant under heterotrophic conditions. Plant Physiol. 1973, 51, 337–344.
Newman, S.M.; Boynton, J.E.; Gillham, N.W.; Randolph-Anderson, B.L.; Johnson, A.M.; Harris, E.H. Transformation of chloroplast ribosomal RNA genes in Chlamydomonas: Molecular and genetic characterization of integration events. Genetics 1990, 126, 875–888.
Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120.
Merchant, S.S.; Prochnik, S.E.; Vallon, O.; Harris, E.H.; Karpowicz, S.J.; Witman, G.B.; Terry, A.; Salamov, A.; Fritz-Laylin, L.K.; Maréchal-Drouard, L.; et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007, 318, 245–250.
Trapnell, C.; Roberts, A.; Goff, L.; Pertea, G.; Kim, D.; Kelley, D.R.; Pimentel, H.; Salzberg, S.L.; Rinn, J.L.; Pachter, L. TopHat and Cufflinks_Protocol. Nat. Protoc. 2012, 7, 562–578.
Tenenbaum, D. KEGGREST: Client-Side REST Access to KEGG. R Package Version 1.24.0.; 2019.
Terauchi, A.M.; Peers, G.; Kobayashi, M.C.; Niyogi, K.K.; Merchant, S.S. Trophic status of Chlamydomonas reinhardtii influences the impact of iron deficiency on photosynthesis. Photosynth. Res. 2010, 105, 39–49.
Willamme, R.; Bogaert, K.A.; Remacle, F.; Remacle, C. Surprisal analysis of the transcriptomic response of the green microalga Chlamydomonas to the addition of acetate during day/night cycles. Chem. Phys. 2018, 514, 154–163.
Berger, H.; Blifernez-Klassen, O.; Ballottari, M.; Bassi, R.; Wobbe, L.; Kruse, O. Integration of carbon assimilation modes with photosynthetic light capture in the green alga Chlamydomonas reinhardtii. Mol. Plant 2014, 7, 1545–1559.
Berger, H.; De Mia, M.; Morisse, S.; Marchand, C.H.; Lemaire, S.D.; Wobbe, L.; Kruse, O. A light switch based on protein s-nitrosylation fine-tunes photosynthetic light harvesting in Chlamydomonas. Plant Physiol. 2016, 171, 821–832.
Tokutsu, R.; Fujimura-Kamada, K.; Matsuo, T.; Yamasaki, T.; Minagawa, J. The CONSTANS flowering complex controls the protective response of photosynthesis in the green alga Chlamydomonas. Nat. Commun. 2019, 10, 4099.
Gabilly, S.T.; Baker, C.R.; Wakao, S.; Crisanto, T.; Guan, K.; Bi, K.; Guiet, E.; Guadagno, C.R.; Niyogi, K.K. Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS. Proc. Natl. Acad. Sci. USA 2019, 116, 17556–17562.
Fukuzawa, H.; Miura, K.; Ishizaki, K.; Kucho, K.I.; Saito, T.; Kohinata, T.; Ohyama, K. Ccm1, a regulatory gene controlling the induction of a carbon-concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability. Proc. Natl. Acad. Sci. USA 2001, 98, 5347–5352.
Fang, W.; Si, Y.; Douglass, S.; Casero, D.; Merchant, S.S.; Pellegrini, M.; Ladunga, I.; Liu, P.; Spalding, M.H. Transcriptome-wide changes in Chlamydomonas reinhardtii gene expression regulated by carbon dioxide and the CO2-concentrating mechanism regulator CIA5/CCM1. Plant Cell 2012, 24, 1876–1893.
Pollock, S.V.; Colombo, S.L.; Prout, D.L.; Godfrey, A.C.; Moroney, J.V. Rubisco activase is required for optimal photosynthesis in the green alga Chlamydomonas reinhardtii in a low-CO2 atmosphere. Plant Physiol. 2003, 133, 1854–1861.
Moroney, J.V.; Kitayama, M.; Togasaki, R.K.; Tolbert, N.E. Evidence for inorganic carbon transport by intact chloroplasts of Chlamydomonas reinhardtii. Plant Physiol. 1987, 83, 460–463.
Gasch, A.P.; Spellman, P.T.; Kao, C.M.; Carmel-Harel, O.; Eisen, M.B.; Storz, G.; Botstein, D.; Brown, P.O. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 2000, 11, 4241–4257.
Hosono, K.; Sasaki, T.; Minoshima, S.; Shimizu, N. Identification and characterization of a novel gene family YPEL in a wide spectrum of eukaryotic species. Gene 2004, 340, 31–43.
Kelley, K.D.; Miller, K.R.; Todd, A.; Kelley, A.R.; Tuttle, R.; Berberich, S.J. YPEL3, a p53-regulated gene that induces cellular senescence. Cancer Res. 2010, 70, 3566–3575.
Piras, V.; Selvarajoo, K. The reduction of gene expression variability from single cells to populations follows simple statistical laws. Genomics 2015, 105, 137–144.
Gross, A.; Levine, R.D. Surprisal analysis of transcripts expression levels in the presence of noise: A reliable determination of the onset of a tumor phenotype. PLoS ONE 2013, 8, e61554.
