Ribosome profiling in the Symbiodiniacean dinoflagellate Fugacium kawagutii shows coordinated protein synthesis of enzymes in different pathways at different times of day.
cell metabolism
dinoflagellates
protein synthesis rates
ribosome profiling
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
revised:
19
07
2023
received:
25
04
2023
accepted:
21
07
2023
medline:
25
9
2023
pubmed:
7
8
2023
entrez:
7
8
2023
Statut:
ppublish
Résumé
Dinoflagellates respond to daily changes in light and dark by changes in cellular metabolism, yet the mechanisms used are still unclear. For example, Fugacium (previously Symbiodinium) kawagutii shows little difference in the transcriptome between day and night suggesting little transcriptional control over gene expression. Here, we have performed ribosome profiling at 2 h intervals over a daily light-dark cycle to assess the degree to which protein synthesis rates might change over the daily cycle. The number of F. kawagutii coding sequences with significant differences in the number of ribosome-protected fragments (RPF) over the 24-h cycle was 2923 using JTK_Cycle and 3655 using ECHO. The majority of the regulated transcripts showed peak translation at the onset of the dark period. The regulated sequences were assigned to different KEGG pathways and transcripts that were translated at roughly the same time were termed concurrently regulated. Both analyses revealed concurrent regulation of many transcripts whose gene products were involved in spliceosome or lysosome biogenesis with peak translation rates around the onset of the dark period, while others, involved in nitrate metabolism and ribosomal proteins, were preferentially translated around the onset of the day phase or the end of the night phase, respectively. In addition, some sequences involved in DNA synthesis were preferentially translated at the end of the day. We conclude that light-dark cycles seem able to synchronize translation of some transcripts encoding proteins involved in a range of different cellular processes, and propose that these changes may help the cells adapt and alter their metabolism as a function of the time of day.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
462-471Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Beauchemin, M. & Morse, D. (2017) A proteomic portrait of dinoflagellate chromatin reveals abundant RNA-binding proteins. Chromosoma, 127, 1-15.
Bodansky, S., Mintz, L.B. & Holmes, D.S. (1979) The mesokaryote Gyrodinium cohnii lacks nucleosomes. Biochemical and Biophysical Research Communications, 88, 1329-1336.
Bowazolo, C. & Morse, D. (2023) Insights into daily metabolic changes of the dinoflagellate Lingulodinium from ribosome profiling. Cell Cycle, 22, 1343-1352.
Bowazolo, C., Song, B., Dorion, S., Beauchemin, M., Chevrier, S., Rivoal, J. et al. (2022) Orchestrated translation specializes dinoflagellate metabolism three times per day. Proceedings of the National Academy of Sciences of the United States of America, 119, e2122335119.
Bowazolo, C., Tse, S.P.K., Beauchemin, M., Lo, S.C., Rivoal, J. & Morse, D. (2020) Label-free MS/MS analyses of the dinoflagellate Lingulodinium identifies rhythmic proteins facilitating adaptation to a diurnal LD cycle. Science of the Total Environment, 704, 135430.
Dagenais-Bellefeuille, S., Bertomeu, T. & Morse, D. (2008) S-phase and M-phase timing are under independent circadian control in the dinoflagellate Lingulodinium. Journal of Biological Rhythms, 23, 400-408.
De Los Santos, H., Collins, E.J., Mann, C., Sagan, A.W., Jankowski, M.S., Bennett, K.P. et al. (2020) ECHO: an application for detection and analysis of oscillators identifies metabolic regulation on genome-wide circadian output. Bioinformatics, 36, 773-781.
El-Athman, R., Knezevic, D., Fuhr, L. & Relogio, A. (2019) A computational analysis of alternative splicing across mammalian tissues reveals circadian and Ultradian rhythms in splicing events. International Journal of Molecular Sciences, 20, 3977.
Genov, N., Basti, A., Abreu, M., Astaburuaga, R. & Relogio, A. (2019) A bioinformatic analysis identifies circadian expression of splicing factors and time-dependent alternative splicing events in the HD-MY-Z cell line. Scientific Reports, 9, 11062.
Gornik, S.G., Ford, K.L., Mulhern, T.D., Bacic, A., McFadden, G.I. & Waller, R.F. (2012) Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates. Current Biology, 22, 2303-2312.
Guillard, R.R.L. & Ryther, J.H. (1962) Studies on marine planktonic diatoms: Cyclotella nana Hufstedt and Denotula confervacea (Cleve) Gran. Canadian Journal of Microbiology, 8, 229-239.
Herzog, M. & Soyer, M.-O. (1981) Distinctive features of dinoflagellate chromatin. Absense of nucleosomes in a primitive species Prorocentrum micans. European Journal of Cell Biology, 23, 295-302.
Holm-Hansen, O. (1969) Algae: amounts of DNA and carbon in single cells. Science, 163, 87-88.
Hughes, M.E., Abruzzi, K.C., Allada, R., Anafi, R., Arpat, A.B., Asher, G. et al. (2017) Guidelines for genome-scale analysis of biological rhythms. Journal of Biological Rhythms, 32, 380-393.
Hughes, M.E., Hogenesch, J.B. & Kornacker, K. (2010) JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. Journal of Biological Rhythms, 25, 372-380.
Iadevaia, V., Caldarola, S., Tino, E., Amaldi, F. & Loreni, F. (2008) All translation elongation factors and the e, f, and h subunits of translation initiation factor 3 are encoded by 5′-terminal oligopyrimidine (TOP) mRNAs. RNA, 14, 1730-1736.
Ingolia, N.T. (2016) Ribosome footprint profiling of translation throughout the genome. Cell, 165, 22-33.
Ingolia, N.T., Ghaemmaghami, S., Newman, J.R. & Weissman, J.S. (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science, 324, 218-223.
Kanehisa, M., Sato, Y. & Morishima, K. (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. Journal of Molecular Biology, 428, 726-731.
LaJeunesse, T.C., Parkinson, J.E., Gabrielson, P.W., Jeong, H.J., Reimer, J.D., Voolstra, C.R. et al. (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Current Biology, 28, 2570-2580.e6.
Leveson, A.C. & Wong, J.T.Y. (1999) PCNA proteins in dinoflagellates. Journal of Phycology, 35, 798-805.
Li, T., Yu, L., Song, B., Song, Y., Li, L., Lin, X. et al. (2020) Genome improvement and Core gene set refinement of Fugacium kawagutii. Microorganisms, 8, 102.
Lin, S., Cheng, S., Song, B., Zhong, X., Lin, X., Li, W. et al. (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science, 350, 691-694.
Markovic, P., Roenneberg, T. & Morse, D. (1996) Phased protein synthesis at several circadian times does not change protein levels in Gonyaulax. Journal of Biological Rhythms, 11, 57-67.
Milos, P., Morse, D. & Hastings, J.W. (1990) Circadian control over synthesis of many Gonyaulax proteins is at a translational level. Naturwiss, 77, 87-89.
Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T. & Ohsumi, Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Molecular Biology of the Cell, 15, 1101-1111.
Morey, J.S. & van Dolah, F.M. (2013) Global analysis of mRNA half-lives and de novo transcription in a dinoflagellate, Karenia brevis. PLoS One, 8, e66347.
Morse, D., Hastings, J.W. & Roenneberg, T. (1994) Different phase responses of the two circadian oscillators in Gonyaulax. Journal of Biological Rhythms, 9, 263-274.
Patro, R., Duggal, G., Love, M.I., Irizarry, R.A. & Kingsford, C. (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nature Methods, 14, 417-419.
Ramalho, C.B., Hastings, J.W. & Colepicolo, P. (1995) Circadian oscillation of nitrate reductase activity in Gonyaulax polyedra is due to changes in cellular protein levels. Plant Physiology, 107, 225-231.
Reid, D.W., Shenolikar, S. & Nicchitta, C.V. (2015) Simple and inexpensive ribosome profiling analysis of mRNA translation. Methods, 91, 69-74.
Riaz, S., Sui, Z., Niaz, Z., Khan, S., Liu, Y. & Liu, H. (2018) Distinctive nuclear features of dinoflagellates with a particular focus on histone and histone-replacement proteins. Microorganisms, 6, 128.
Roenneberg, T. & Morse, D. (1993) Two circadian clocks in a single cell. Nature, 362, 362-364.
Romanowski, A., Schlaen, R.G., Perez-Santangelo, S., Mancini, E. & Yanovsky, M.J. (2020) Global transcriptome analysis reveals circadian control of splicing events in Arabidopsis thaliana. The Plant Journal: For Cell and Molecular Biology, 103, 889-902.
Roy, S., Beauchemin, M., Dagenais-Bellefeuille, S., Letourneau, L., Cappadocia, M. & Morse, D. (2014) The Lingulodinium circadian system lacks rhythmic changes in transcript abundance. BMC Biology, 12, 107.
Roy, S. & Morse, D. (2012) A full suite of histone and histone modifying genes are transcribed in the dinoflagellate Lingulodinium. PLoS One, 7, e34340.
Schnepf, E. & Elbrachter, M. (1992) Nutritional strategies in dinoflagellates: a review with emphasis on cell biological aspects. European Journal of Protistology, 28, 3-24.
Sorek, M., Yacobi, Y.Z., Roopin, M., Berman-Frank, I. & Levy, O. (2013) Photosynthetic circadian rhythmicity patterns of Symbiodinium, the coral endosymbiotic algae. Proceedings of the Royal Society B, 280, 20122942.
Toledo, M., Batista-Gonzalez, A., Merheb, E., Aoun, M.L., Tarabra, E., Feng, D. et al. (2018) Autophagy regulates the liver clock and glucose metabolism by degrading CRY1. Cell Metabolism, 28, 268-281 e264.
Walker, S.E. & Lorsch, J. (2013) RNA purification-Precipitation methods. Methods in Enzymology, 530, 337-343.
Wang, D.Z., Zhang, Y.J., Zhang, S.F., Lin, L. & Hong, H.S. (2013) Quantitative proteomic analysis of cell cycle of the dinoflagellate Prorocentrum donghaiense (Dinophyceae). PLoS One, 8, e63659.
Wang, L.-H., Liu, Y.-H., Ju, Y.-M., Hsiao, Y.-Y., Fang, L.-S. & Chen, C.-S. (2008) Cell cycle propagation is driven by light-dark stimulation in a cultured symbiotic dinoflagellate isolated from corals. Coral Reefs, 27, 823-835.
Yoshihama, M., Uechi, T., Asakawa, S., Kawasaki, K., Kato, S., Higa, S. et al. (2002) The human ribosomal protein genes: sequencing and comparative analysis of 73 genes. Genome Research, 12, 379-390.
Yu, L., Li, T., Li, L., Lin, X., Li, H., Liu, C. et al. (2020) SAGER: a database of Symbiodiniaceae and algal genomic resource. Database: The Journal of Biological Databases and Curation, 2020, baaa051.
Zaheri, B., Dagenais-Bellefeuille, S., Song, B. & Morse, D. (2019) Assessing transcriptional responses to light by the dinoflagellate Symbiodinium. Microorganisms, 7(8), 261. doi: 10.3390/microorganisms7080261.
Zaheri, B. & Morse, D. (2022) An overview of transcription in dinoflagellates. Gene, 829, 146505.
Zhang, H., Hou, Y. & Lin, S. (2006) Isolation and characterization of proliferating cell nuclear antigen from the dinoflagellate Pfiesteria piscicida. The Journal of Eukaryotic Microbiology, 53, 142-150.
Zhang, H., Hou, Y., Miranda, L., Campbell, D.A., Sturm, N.R., Gaasterland, T. et al. (2007) Spliced leader RNA trans-splicing in dinoflagellates. Proceedings. National Academy of Sciences. United States of America, 104, 4618-4623.
Zhang, H., Zhou, Y., Liu, T.Q., Yin, X.J., Lin, L., Lin, Q. et al. (2021) Initiation of efficient C(4) pathway in response to low ambient CO(2) during the bloom period of a marine dinoflagellate. Environmental Microbiology, 23, 3196-3211.
Zhou, J. & Fritz, L. (1994) The PAS/accumulation bodies in Prorocentrum lima and prorocentrum maculosum (Dinophyceae) are dinoflagellate lysosomes. Journal of Phycology, 30, 39-44.