To Divide or Not to Divide? How Deuterium Affects Growth and Division of Chlamydomonas reinhardtii

. 2021 Jun 09 ; 11 (6) : . [epub] 20210609

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34207920

Grantová podpora
17-06264S Grantová Agentura České Republiky

Extensive in vivo replacement of hydrogen by deuterium, a stable isotope of hydrogen, induces a distinct stress response, reduces cell growth and impairs cell division in various organisms. Microalgae, including Chlamydomonas reinhardtii, a well-established model organism in cell cycle studies, are no exception. Chlamydomonas reinhardtii, a green unicellular alga of the Chlorophyceae class, divides by multiple fission, grows autotrophically and can be synchronized by alternating light/dark regimes; this makes it a model of first choice to discriminate the effect of deuterium on growth and/or division. Here, we investigate the effects of high doses of deuterium on cell cycle progression in C. reinhardtii. Synchronous cultures of C. reinhardtii were cultivated in growth medium containing 70 or 90% D2O. We characterize specific deuterium-induced shifts in attainment of commitment points during growth and/or division of C. reinhardtii, contradicting the role of the "sizer" in regulating the cell cycle. Consequently, impaired cell cycle progression in deuterated cultures causes (over)accumulation of starch and lipids, suggesting a promising potential for microalgae to produce deuterated organic compounds.

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West J.B., Bowen G.J., Cerling T.E., Ehleringer J.R. Stable isotopes as one of nature’s ecological recorders. Trends Ecol. Evol. 2006;21:408–414. doi: 10.1016/j.tree.2006.04.002. PubMed DOI

Berg T., Strand D.H. 13C labelled internal standards—A solution to minimize ion suppression effects in liquid chromatography-tandem mass spectrometry analyses of drugs in biological samples? J. Chromatogr. A. 2011;1218:9366–9374. doi: 10.1016/j.chroma.2011.10.081. PubMed DOI

Lehmann W.D. A timeline of stable isotopes and mass spectrometry in the life sciences. Mass Spectrom. Rev. 2017;36:58–85. doi: 10.1002/mas.21497. PubMed DOI

Hirakura Y., Sugiyama T., Takeda M., Ikeda M., Yoshioka T. Deuteration as a tool in investigating the role of protons in cell signaling. Biochim. Biophys. Acta. 2011;1810:218–225. doi: 10.1016/j.bbagen.2010.10.005. PubMed DOI

Salomonsson L., Branden G., Brzezinski P. Deuterium isotope effect of proton pumping in cytochrome c oxidase. Biochim. Biophys. Acta. 2008;1777:343–350. doi: 10.1016/j.bbabio.2007.09.009. PubMed DOI

Olgun A. Biological effects of deuteronation: ATP synthase as an example. Theor. Biol. Med. Model. 2007;4 doi: 10.1186/1742-4682-4-9. PubMed DOI PMC

de Kouchkovsky Y., Haraux F., Sigalat C. Effect of hydrogen-deuterium exchange on energy-coupled processes in thylakoids. FEBS Lett. 1982;139:245–249. doi: 10.1016/0014-5793(82)80862-4. DOI

Fuks B., Homblé F. Mechanism of proton permeation through chloroplast lipid membranes. Plant Physiol. 1996;112:759–766. doi: 10.1104/pp.112.2.759. PubMed DOI PMC

Gross P.R., Spindel W. Mitotic arrest by deuterium oxide. Science. 1960;131:37–39. doi: 10.1126/science.131.3392.37. PubMed DOI

Takeda H., Nio Y., Omori H., Uegaki K., Hirahara N., Sasaki S., Tamura K., Ohtani H. Mechanisms of cytotoxic effects of heavy water (deuterium oxide: D2O) on cancer cells. Anti-Cancer Drugs. 1998;9:715–725. doi: 10.1097/00001813-199809000-00007. PubMed DOI

Evans B.R., Bali G., Reeves D.T., O’Neill H.M., Sun Q., Shah R., Ragauskas A.J. Effect of D2O on growth properties and chemical structure of annual ryegrass (Lolium multiflorum) J. Agric. Food Chem. 2014;62:2595–2604. doi: 10.1021/jf4055566. PubMed DOI

Sacchi G.A., Cocucci M. Effects of deuterium oxide on growth, proton extrusion, potassium influx, and in vitro plasma membrane activities in maize root segments. Plant Physiol. 1992;100:1962–1967. doi: 10.1104/pp.100.4.1962. PubMed DOI PMC

Mosin O., Ignatov I., Skladnev D., Shvets V. Studying of phenomenon of biological adaptation to heavy water. Eur. J. Mol. Biotechnol. 2014;6:180–209.

Hirai K., Tomida M., Kikuchi Y., Ueda O., Ando H., Asanuma N. Effects of deuterium oxide on Streptococcus mutans and Pseudomonas aeruginosa. Bull. Tokyo Dent. Coll. 2010;51:175–183. doi: 10.2209/tdcpublication.51.175. PubMed DOI

Haon S., Auge S., Tropis M., Milon A.J. Low cost production of perdeuterated biomass using methylotrophic yeasts. J. Labelled Compd. Rad. 1993;22:1053–1063. doi: 10.1002/jlcr.2580331108. DOI

Bhosale P., Serban B., Bernstein P.S. Production of deuterated lutein by Chlorella protothecoides and its detection by mass spectrometric methods. Biotechnol. Lett. 2006;28:1371–1375. doi: 10.1007/s10529-006-9105-8. PubMed DOI

Zachleder V., Vítová M., Hlavová M., Moudříková Š., Mojzeš P., Heumann H., Becher J.R., Bišová K. Stable isotope compounds—production, detection, and application. Biotechnol. Adv. 2018;36:784–797. doi: 10.1016/j.biotechadv.2018.01.010. PubMed DOI

Lewis G.N. The biochemistry of water containing hydrogen isotope. J. Am. Chem. Soc. 1933;55:3503–3504. doi: 10.1021/ja01335a509. DOI

Lewis G.N. The biology of heavy water. Science. 1934;79:151–153. doi: 10.1126/science.79.2042.151. PubMed DOI

Hlavová M., Vítová M., Bišová K. Synchronization of green algae by light and dark regimes for cell cycle and cell division studies. In: Caillaud M.-C., editor. Plant Cell Division. Springer Science; Berlin/Heidelberg, Germany: 2016. pp. 3–16. PubMed

Howard A., Pelc S.R. Synthesis of deoxyribonucleic acid in normal and irradiated cells and its relation to chromosome breakage. Heredity. 1953;6:261–273.

Lien T., Knutsen G. Synchronous growth of Chlamydomonas reinhardtii (Chlorophyceae): A review of optimal conditions. J. Phycol. 1979;15:191–200. doi: 10.1111/j.1529-8817.1979.tb02984.x. DOI

Donnan L., John P.C.L. Cell cycle control by timer and sizer in Chlamydomonas. Nature. 1983;304:630–633. doi: 10.1038/304630a0. PubMed DOI

Zachleder V., Bišová K., Vítová M. The cell cycle of microalgae. In: Borowitzka M.A., Beardall J., Raven J.A., editors. The physiology of Microalgae. Volume 6. Springer; Berlin/Heidelberg, Germany: 2016. pp. 3–46.

Bisova K., Zachleder V. Cell-cycle regulation in green algae dividing by multiple fission. J. Exp. Bot. 2014;65:2585–2602. doi: 10.1093/jxb/ert466. PubMed DOI

Kselíková V., Zachleder V., Bišová K. Analysis of commitment point attainment in algae dividing by multiple fission. In: Caillaud M.-C., editor. Plant Cell Division. Springer US; New York, NY, USA: 2021. PubMed DOI

Bisova K., Krylov D.M., Umen J.G. Genome-wide annotation and expression profiling of cell cycle regulatory genes in Chlamydomonas reinhardtii. Plant Physiol. 2005;137:475–491. doi: 10.1104/pp.104.054155. PubMed DOI PMC

Bišová K. Assaying cyclin-dependent kinase activity in synchronized algal cultures. In: Caillaud M.-C., editor. Plant Cell Division. Springer US; New York, NY, USA: 2021. PubMed DOI

Langan T.A., Gautier J., Lohka M., Hollingsworth R., Moreno S., Nurse P., Maller J., Sclafani R.A. Mammalian growth-associated H1 histone kinase: A homologue of cdc2+/CDC28 protein kinases controlling mitotic entry in yeast and frog cells. Mol. Cell. Biol. 1989;9:3860–3868. doi: 10.1128/MCB.9.9.3860. PubMed DOI PMC

Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. PubMed DOI

Zachleder V., Ivanov I., Vítová M., Bišová K. Cell cycle arrest by supraoptimal temperature in the alga Chlamydomonas reinhardtii. Cells. 2019;8:1237. doi: 10.3390/cells8101237. PubMed DOI PMC

McCready R.M., Guggolz J., Silviera V., Owens H.S. Determination of starch and amylose in vegetables. Anal. Chem. 1950;22:1156–1158. doi: 10.1021/ac60045a016. DOI

Brányiková I., Maršálková B., Doucha J., Brányik T., Bišová K., Zachleder V., Vítová M. Microalgae-novel highly efficient starch producers. Biotechnol. Bioeng. 2011;108:766–776. doi: 10.1002/bit.23016. PubMed DOI

Takeshita T., Takeda K., Ota S., Yamazaki T., Kawano S. A simple method for measuring the starch and ĺipid contents in the cell of microalgae. Cytologia. 2015;80:475–481. doi: 10.1508/cytologia.80.475. DOI

Unno K., Hagima N., Kishido T., Okada S., Oku N. Deuterium-resistant algal cell line for D labeling of heterotrophs expresses enhanced level of Hsp60 in D2O medium. Appl. Environ. Microbiol. 2005;71:2256–2259. doi: 10.1128/AEM.71.5.2256-2259.2005. PubMed DOI PMC

Chorney W., Scully N.J., Crespi H.L., Katz J.J. The growth of algae in deuterium oxide. Biochim. Biophys. Acta. 1960;37:280–287. doi: 10.1016/0006-3002(60)90235-3. PubMed DOI

Kushner D.J., Baker A., Dunstall T.G. Biotechnological potential of heavy water and deuterated compounds; Proceedings of the Biotechnology Risk Assessment Symposium; Ottawa, ON, Canada. 23–25 June 1996; pp. 75–89.

Gireesh T., Jayadeep A., Rajasekharan K.N., Menon V.P., Vairamany M., Tang G., Nair P.P., Sudhakaran P.R. Production of deuterated β-carotene by metabolic labelling of Spirulina platensis. Biotechnol. Lett. 2001;23:447–449. doi: 10.1023/A:1010378401621. DOI

Kollars B., Geraets R. Effects of deuterium on Chlamydomonas reinhardtii. J. Undergrad. Res. 2008;6:113–117.

de Carpentier F., Lemaire S.D., Danon A. When Unity Is Strength: The Strategies Used by Chlamydomonas to Survive Environmental Stresses. Cells. 2019;8:1307. doi: 10.3390/cells8111307. PubMed DOI PMC

Moses V., Holm-Hansen O., Calvin M. Response of Chlorella to a deuterium environment. Biochim. Biophys. Acta. 1958;28:62–70. doi: 10.1016/0006-3002(58)90428-1. PubMed DOI

Crespi H.L., Conrad S.M., Uphaus R.A., Katz J.J. Cultivation of microorganisms in heavy water. Annal. N. Y. Acad. Sci. 1960;84:648–666. doi: 10.1111/j.1749-6632.1960.tb39098.x. PubMed DOI

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. doi: 10.1093/pcp/pcs082. PubMed DOI

Cakmak T., Angun P., Demiray Y.E., Ozkan A.D., Elibol Z., Tekinay T. Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol. Bioeng. 2012;109:1947–1957. doi: 10.1002/bit.24474. PubMed DOI

Li Y., Han D., Hu G., Sommerfeld M., Hu Q. Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol. Bioeng. 2010;107:258–268. doi: 10.1002/bit.22807. PubMed DOI

Atikij T., Syaputri Y., Iwahashi H., Praneenararat T., Sirisattha S., Kageyama H., Waditee-Sirisattha R. Enhanced lipid production and molecular dynamics under salinity stress in green microalga Chlamydomonas reinhardtii (137C) Mar. Drugs. 2019;17:484. doi: 10.3390/md17080484. PubMed DOI PMC

Legeret B., Schulz-Raffelt M., Nguyen H.M., Auroy P., Beisson F., Peltier G., Blanc G., Li-Beisson Y. Lipidomic and transcriptomic analyses of Chlamydomonas reinhardtii under heat stress unveil a direct route for the conversion of membrane lipids into storage lipids. Plant Cell Environ. 2016;39:834–847. doi: 10.1111/pce.12656. PubMed DOI

Goold H.D., Cuine S., Legeret B., Liang Y., Brugiere S., Auroy P., Javot H., Tardif M., Jones B.J., Beisson F., et al. Saturating light induces sustained accumulation of oil in plastidal lipid droplets in Chlamydomonas reinhardtii. Plant Physiol. 2016;171:2406–2417. doi: 10.1104/pp.16.00718. PubMed DOI PMC

Fernandes B., Teixeira J., Dragone G., Vicente A.A., Kawano S., Bišová K., Přibyl P., Zachleder V., Vítová M. Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri. Bioresour. Technol. 2013;144:268–274. doi: 10.1016/j.biortech.2013.06.096. PubMed DOI

Takeshita T., Ota S., Yamazaki T., Hirata A., Zachleder V., Kawano S. Starch and lipid accumulation in eight strains of six Chlorella species under comparatively high light intensity and aeration culture conditions. Bioresour. Technol. 2014;158:127–134. doi: 10.1016/j.biortech.2014.01.135. PubMed DOI

Pick U., Avidan O. Triacylglycerol is produced from starch and polar lipids in the green alga Dunaliella tertiolecta. J. Exp. Bot. 2017;68:4939–4950. doi: 10.1093/jxb/erx280. PubMed DOI PMC

Yang J. Deuterium: Discovery and Applications in Organic Chemistry. Elsevier; Amsterdam, The Netherlands: 2016.

Katz J.J., Crespi H.L. Deuterated organisms: Cultivation and uses. Science. 1966;151:1187–1194. doi: 10.1126/science.151.3715.1187. PubMed DOI

Vítová M., Bišová K., Umysová D., Hlavová M., Kawano S., Zachleder V., Čížková M. Chlamydomonas reinhardtii: Duration of its cell cycle and phases at growth rates affected by light intensity. Planta. 2011;233:75–86. doi: 10.1007/s00425-010-1282-y. PubMed DOI

Vítová M., Bišová K., Hlavová M., Kawano S., Zachleder V., Čížková M. Chlamydomonas reinhardtii: Duration of its cell cycle and phases at growth rates affected by temperature. Planta. 2011;234:599–608. doi: 10.1007/s00425-011-1427-7. PubMed DOI

Mihara S., Hase E. Studies on the vegetative life cycle of Chlamydomonas reinhardi Dangeard in synchronous culture II. Effects of chloramphenicol and cycloheximide on the length of cell cycle. Plant Cell Physiol. 1971;12:237–241.

Zachleder V., Bišová K., Vítová M.Š.K.J.H. Variety of cell cycle patterns in the alga Scenedesmus quadricauda (Chlorophyta) as revealed by application of illumination regimes and inhibitors. Eur. J. Phycol. 2002;37:361–371. doi: 10.1017/S0967026202003815. DOI

Zachleder V., Schläfli O., Boschetti A. Growth-controlled oscillation in activity of histone H1 kinase during the cell cycle of Chlamydomonas reinhardtii (Chlorophyta) J. Phycol. 1997;33:673–681. doi: 10.1111/j.0022-3646.1997.00673.x. DOI

Čížková M., Pichová A., Vítová M., Hlavová M., Hendrychová J., Umysová D., Gálová E., Ševčovičová A., Zachleder V., Umen J.G., et al. CDKA and CDKB kinases from Chlamydomonas reinhardtii are able to complement cdc28 temperature-sensitive mutants of Saccharomyces cerevisiae. Protoplasma. 2008;232:183–191. doi: 10.1007/s00709-008-0285-z. PubMed DOI

Zachleder V., Ivanov I., Vítová M., Bišová K. Effects of cyclin-dependent kinase activity on the coordination of growth and the cell cycle in green algae at different temperatures. J. Exp. Bot. 2019;70:845–858. doi: 10.1093/jxb/ery391. PubMed DOI

Cross F.R., Umen J.G. The Chlamydomonas cell cycle. Plant J. 2015;82:370–392. doi: 10.1111/tpj.12795. PubMed DOI PMC

John P.C.L., Donnan L., Harper J.D.I., Rollins M.J., Keenan C.A. Control of cell division in Chlorella and Chlamydomonas; Proceedings of the 6th European Cell Cycle Workshop Progress in Cell Cycle Controls; Prague. Czech Republic; 1983; pp. 81–95.

Howell S.H., Blaschko W.J., Drew C.M. Inhibitor effects during cell-cycle in Chlamydomonas reinhardtii—determination of transition points in asynchronous cultures. J. Cell Biol. 1975;67:126–135. doi: 10.1083/jcb.67.1.126. PubMed DOI PMC

Panda D., Chakrabarti G., Hudson J., Pigg K., Miller H.P., Wilson L., Himes R.H. Suppression of microtubule dynamic instability and treadmilling by deuterium oxide. Biochemistry. 2000;39:5075–5081. doi: 10.1021/bi992217f. PubMed DOI

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