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Supra-Optimal Temperature: An Efficient Approach for Overaccumulation of Starch in the Green Alga Parachlorella kessleri

. 2021 Jul 16 ; 10 (7) : . [epub] 20210716

Language English Country Switzerland Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Grant support
17-06264S Grantová Agentura České Republiky
AVOZ61388971 Institutional Research Concept

Green algae are fast-growing microorganisms that are considered promising for the production of starch and neutral lipids, and the chlorococcal green alga Parachlorella kessleri is a favorable model, as it can produce both starch and neutral lipids. P. kessleri commonly divides into more than two daughter cells by a specific mechanism-multiple fission. Here, we used synchronized cultures of the alga to study the effects of supra-optimal temperature. Synchronized cultures were grown at optimal (30 °C) and supra-optimal (40 °C) temperatures and incident light intensities of 110 and 500 μmol photons m-2 s-1. The time course of cell reproduction (DNA replication, cellular division), growth (total RNA, protein, cell dry matter, cell size), and synthesis of energy reserves (net starch, neutral lipid) was studied. At 40 °C, cell reproduction was arrested, but growth and accumulation of energy reserves continued; this led to the production of giant cells enriched in protein, starch, and neutral lipids. Furthermore, we examined whether the increased temperature could alleviate the effects of deuterated water on Parachlorella kessleri growth and division; results show that supra-optimal temperature can be used in algal biotechnology for the production of protein, (deuterated) starch, and neutral lipids.

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Zachleder V., Bišová K., Vítová M., Štěpán K., Hendrychová J. 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

Oldenhof H., Zachleder V., van den Ende H. Blue- and red-light regulation of the cell cycle in Chlamydomonas reinhardtii (Chlorophyta) Eur. J. Phycol. 2006;41:313–320. doi: 10.1080/09670260600699920. DOI

Oldenhof H., Zachleder V., van den Ende H. Blue light delays commitment to cell division in Chlamydomonas reinhardtii. Plant Biol. 2004;6:689–695. doi: 10.1055/s-2004-821341. PubMed DOI

Munzner P., Voigt J. Blue light regulation of cell division in Chlamydomonas reinhardtii. Plant Physiol. 1992;99:1370–1375. doi: 10.1104/pp.99.4.1370. PubMed DOI PMC

Voigt J., Munzner P. The Chlamydomonas cell-cycle is regulated by a light dark- responsive cell-cycle switch. Planta. 1987;172:463–472. doi: 10.1007/BF00393861. PubMed DOI

McAteer M., Donnan L., John P.C.L. The timing of division in Chlamydomonas. New Phytol. 1985;99:41–56. doi: 10.1111/j.1469-8137.1985.tb03635.x. DOI

Donnan L., Carvill E.P., Gilliland T.J., John P.C.L. The cell-cycles of Chlamydomonas and Chlorella. New Phytol. 1985;99:1–40. doi: 10.1111/j.1469-8137.1985.tb03634.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., Šetlík I. Timing of events in overlapping cell reproductive sequences and their mutual interactions in the alga Scenedesmus quadricauda. J. Cell Sci. 1990;97:631–638. doi: 10.1242/jcs.97.4.631. DOI

Los D.A., Zachleder V., Kuptsova E.S., Ksenofontov A.L., Markelova A.G., Shapiguzov Y.M., Semenenko V.E. Effect of the spectral composition of light on replication of chloroplast DNA and division of chloroplast nucleoids in the green-alga Dunaliella salina. Russ. Plant Physiol. 1990;37:791–798.

Morimura Y. Synchronous culture of Chlorella. I. Kinetic analysis of the life cycle of Chlorella ellipsoidea as affected by changes of temperature and light intensity. Plant Cell Physiol. 1959;1:49–62.

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

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

Zachleder V., van den Ende H. Cell cycle events in the green alga Chlamydomonas eugametos and their control by environmental factors. J. Cell Sci. 1992;102:469–474. doi: 10.1242/jcs.102.3.469. 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

Bišová K., Hendrychová J., Cepák V., Zachleder V. Cell growth and division processes are differentially sensitive to cadmium in Scenedesmus quadricauda. Folia Microbiol. 2003;48:805–816. doi: 10.1007/BF02931518. PubMed DOI

Zachleder V., Ivanov I., Vítová M., Bišová K. Cell cycle arrest by supraoptimal temperature in the alga Chlamydomonas reinhardtii. Cells. 2019;8:1237–1257. doi: 10.3390/cells8101237. PubMed DOI PMC

Šetlík I., Zachleder V., Doucha J., Berková E., Bartoš J. The nature of temperature block in the sequence of reproductive processes in Chlorella vulgaris BEIJERINCK. Arch. Hydrobiol. Suppl. 49 Algol. Stud. 1975;14:70–104.

Krienitz L., Hegewald E.H., Hepperle D., Huss V.A.R., Rohr T., Wolf M. Phylogenetic relationship of Chlorella and Parachlorella gen nov (Chlorophyta, Trebouxiophyceae) Phycologia. 2004;43:529–542. doi: 10.2216/i0031-8884-43-5-529.1. DOI

Řezanka T., Podojil M. The very long-chain fatty-acids of the green-alga Chlorella kessleri. Lipids. 1984;19:472–473. doi: 10.1007/BF02537412. DOI

Ota S., Matsuda T., Takeshita T., Yamazaki T., Kazama Y., Abe T., Kawano S. Phenotypic spectrum of Parachlorella kessleri (Chlorophyta) mutants produced by heavy-ion irradiation. Bioresour. Technol. 2013;149:432–438. doi: 10.1016/j.biortech.2013.09.079. PubMed DOI

Ota S., Yoshihara M., Yamazaki T., Takeshita T., Hirata A., Konomi M., Oshima K., Hattori M., Bišová K., Zachleder V., et al. Deciphering the relationship among phosphate dynamics, electron-dense body and lipid accumulation in the green alga Parachlorella kessleri. Sci. Rep. 2016;6:25731. doi: 10.1038/srep25731. 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

Mizuno Y., Sato A., Watanabe K., Hirata A., Takeshita T., Ota S., Sato N., Zachleder V., Tsuzuki M., Kawano S. Sequential accumulation of starch and lipid induced by sulfur deficiency in Chlorella and Parachlorella species. Bioresour. Technol. 2013;129:150–155. doi: 10.1016/j.biortech.2012.11.030. PubMed DOI

Takeshita T., Ivanov I.N., Oshima K., Ishii K., Kawamoto H., Ota S., Yamazaki T., Hirata A., Kazama Y., Abe T., et al. Comparison of lipid productivity of Parachlorella kessleri heavy-ion beam irradiation mutant PK4 in laboratory and 150-L mass bioreactor, identification and characterization of its genetic variation. Algal Res. 2018;35:416–426. doi: 10.1016/j.algal.2018.09.005. DOI

Taleb A., Legrand J., Takache H., Taha S., Pruvost J. Investigation of lipid production by nitrogen-starved Parachlorella kessleri under continuous illumination and day/night cycles for biodiesel application. J. Appl. Phycol. 2017 doi: 10.1007/s10811-017-1286-0. DOI

Rathod J.P., Prakash G., Pandit R., Lali A.M. Agrobacterium-mediated transformation of promising oil-bearing marine algae Parachlorella kessleri. Photosynth. Res. 2013;118:141–146. doi: 10.1007/s11120-013-9930-2. PubMed DOI

Sato N., Tsuzuki M., Kawaguchi A. Glycerolipid synthesis in Chlorella kessleri 11h - I. Existence of a eukaryotic pathway. Biochim. Biophys. Acta. 2003;1633:27–34. doi: 10.1016/S1388-1981(03)00069-6. PubMed DOI

Saleh M.M., Matorin D.N., Zayadan B.K., Todorenko D.A., Lukashov E.P., Gaballah M.M. Differentiation between two strains of microalga Parachlorella kessleri using modern spectroscopic method. Bot. Stud. 2014;55:53. doi: 10.1186/s40529-014-0053-7. PubMed DOI PMC

Zachleder V., Ivanov I.N., Kselíková V., Bialevich V., Vítová M., Ota S., Takeshita T., Kawano S., Bišová K. Characterization of growth and cell cycle events as affected by light intensity in the green alga Parachlorella kessleri, as a new model for cell cycle research. Biomolecules. 2021;11:891. doi: 10.3390/biom11060891. PubMed DOI PMC

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

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

Torres-Romero I., Kong F., Legeret B., Beisson F., Peltier G., Li-Beisson Y. Chlamydomonas cell cycle mutant crcdc5 over-accumulates starch and oil. Biochimie. 2019 doi: 10.1016/j.biochi.2019.09.017. PubMed DOI

Hirokawa T., Hata M., Takeda H. Correlation between the starch level and the rate of starch synthesis during the development cycle of Chlorella ellipsoidea. Plant Cell Physiol. 1982;23:813–820.

Sorokin C. Changes in photosynthetic activity in the course of cell development in Chlorella. Physiol. Plant. 1957;10:659–666. doi: 10.1111/j.1399-3054.1957.tb06973.x. 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

Izumo A., Fujiwara S., Oyama Y., Satoh A., Fujita N., Nakamura Y., Tsuzuki M. Physicochemical properties of starch in Chlorella change depending on the CO2 concentration during growth: Comparison of structure and properties of pyrenoid and stroma starch. Plant Sci. 2007;172:1138–1147. doi: 10.1016/j.plantsci.2007.03.001. DOI

Ivanov I.N., Zachleder V., Vítová M., Barbosa M.J., Bišová K. Starch production in Chlamydomonas reinhardtii through supraoptimal temperature in a pilot-scale photobioreactor. Cells. 2021;10 doi: 10.3390/cells10051084. PubMed DOI PMC

Li X., Přibyl P., Bišová K., Kawano S., Cepák V., Zachleder V., Čížková M., Brányiková I., Vítová M. The microalga Parachlorella kessleri––a novel highly efficient lipid producer. Biotechnol. Bioeng. 2013;110:97–107. doi: 10.1002/bit.24595. PubMed DOI

Přibyl P., Cepák V., Zachleder V. Production of lipids in 10 strains of Chlorella and Parachlorella, and enhanced lipid productivity in Chlorella vulgaris. Appl. Microbiol. Biotechnol. 2012;94:549–561. doi: 10.1007/s00253-012-3915-5. PubMed DOI

Gao Y., Feng J., Lv J., Liu Q., Nan F., Liu X., Xie S. Physiological changes of Parachlorella kessleri ty02 in lipid accumulation under nitrogen stress. Int. J. Environ. Res. Public Health. 2019;16 doi: 10.3390/ijerph16071188. PubMed DOI PMC

You Z., Zhang Q., Peng Z., Miao X. Lipid droplets mediate salt stress tolerance in Parachlorella kessleri. Plant Physiol. 2019;181:510–526. doi: 10.1104/pp.19.00666. PubMed DOI PMC

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

Yang J. Deuterium: Discovery and applications in organic chemistry. Elsevier; Amsterdam, The Netherlands: 2016.

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

Kinetic isotope effects. [(accessed on 10 June 2021)]; Available online: https://chem.libretexts.org/@go/page/1685.

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

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

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. Agr. 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

Saha S.K., Hayes J., Moane S., Murray P. Tagging of biomolecules with deuterated water (D2O) in commercially important microalgae. Biotechnol. Lett. 2013;35:1067–1072. doi: 10.1007/s10529-013-1176-8. PubMed DOI

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

Cargnin S., Serafini M., Pirali T. A primer of deuterium in drug design. Future Med. Chem. 2019;11:2039–2042. doi: 10.4155/fmc-2019-0183. PubMed DOI

DeWitt S.H., Maryanoff B.E. Deuterated drug nolecules: Focus on FDA-approved deutetrabenazine. Biochemistry. 2018;57:472–473. doi: 10.1021/acs.biochem.7b00765. PubMed DOI

Raffa R.B., Pergolizzi J.V., Taylor R. The First Approved “Deuterated” Drug: A Short Review of the Concept. Pharmacol. Pharm. 2018;09:440–446. doi: 10.4236/pp.2018.910033. DOI

Schmidt C. First deuterated drug approved. Nat. Biotechnol. 2017;35:493–494. doi: 10.1038/nbt0617-493. PubMed DOI

Blake M.I., Crespi H.L., Mohan V., Katz J.J. Isolation of fully deuterated metabolites from Scenedesmus obliquus grown in deuterium oxide. J. Pharm. Sci. 1961;50:425–429. doi: 10.1002/jps.2600500512. DOI

Hattori A., Crespi H.L., Katz J.J. Effect of side-chain deuteration on protein stability. Biochemistry. 1965;4:1213–1225. doi: 10.1021/bi00883a002. PubMed DOI

Closs D.L., Katz J.J., Pennington M.R., Thomas H.R., Strain J. Hydrogen exchange at methine and C-10 positions in chlorophyll. Amer. Chem. Soc. 1963;85:3809. doi: 10.1021/ja00906a020. DOI

Doucha J., Lívanský K. Productivity, CO2/O2 exchange and hydraulics in outdoor open high density microalgal (Chlorella sp.) photobioreactors operated in a Middle and Southern European climate. J. Appl. Phycol. 2006;18:811–826. doi: 10.1007/s10811-006-9100-4. 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

Wanka F. Die bestimmung der nucleinsäuren in Chlorella pyrenoidosa. Planta. 1962;58:594–619. doi: 10.1007/BF01914751. DOI

Lukavský J., Tetík K., Vendlová J. Extraction of nucleic acid from the alga Scenedesmus quadricauda. Arch. Hydrobiol. Suppl. 41 Algol. Stud. 1973;9:416–426.

Decallonne J.R., Weyns C.J. A shortened procedure of the diphenylamine reaction for measurement of deoxyribonucleic acid by using light activation. Anal. Biochem. 1976;74:448–456. doi: 10.1016/0003-2697(76)90225-6. PubMed DOI

Zachleder V. Optimization of nucleic acids assay in green and blue-green algae: Extraction procedures and the light-activated reaction for DNA. Arch. Hydrobiol. Suppl. 67 Algol. Stud. 1984;36:313–328. doi: 10.1127/algol_stud/67/1984/313. DOI

Miller G.L. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 1959;31:426–428. doi: 10.1021/ac60147a030. DOI

Metsoviti M.N., Papapolymerou G., Karapanagiotidis I.T., Katsoulas N. Effect of light intensity and quality on growth rate and composition of Chlorella vulgaris. Plants. 2019;9 doi: 10.3390/plants9010031. PubMed DOI PMC

Barnett J.Z., Foy J., Malone R., Rusch K.A., Gutierrez-Wing M.T. Impact of light quality on a native Louisiana Chlorella vulgaris/Leptolyngbya sp. co-culture. Eng. Life. Sci. 2017;17:678–685. doi: 10.1002/elsc.201600013. PubMed DOI PMC

Borowitzka M.A. Energy from microalgae: A short history. In: Borowitzka M.A., Moheimani N.R., editors. Algae for biofuels and energy. Developments in applied phycology 5. Springer; Dordrecht, The Netherlands: New York, NY, USA: London, UK: 2013. pp. 1–16.

Borowitzka M.A., Raven J.A., Beardall J. In: The physiology of microalgae. 6 ed. Borowitzka M.A., Raven J.A., Beardall J., editors. Springer International Publishing Switzerland; Cham, Germany: Heidelberg, Germany: New York, NY, USA: Dordrecht, The Netherlands: London, UK: 2016. p. 681. DOI

Schuler L., Greque de Morais E., Trovao M., Machado A., Carvalho B., Carneiro M., Maia I., Soares M., Duarte P., Barros A., et al. Isolation and characterization of novel Chlorella vulgaris mutants with low chlorophyll and improved protein contents for food applications. Front. Bioeng. Biotechnol. 2020;8:469. doi: 10.3389/fbioe.2020.00469. PubMed DOI PMC

Al Jabri H., Taleb A., Touchard R., Saadaoui I., Goetz V., Pruvost J. Cultivating microalgae in desert conditions: Evaluation of the effect of light-temperature summer conditions on the growth and metabolism of Nannochloropsis QU130. Appl. Sci. 2021;11 doi: 10.3390/app11093799. DOI

Levin G., Kulikovsky S., Liveanu V., Eichenbaum B., Meir A., Isaacson T., Tadmor Y., Adir N., Schuster G. The desert green algae Chlorella ohadii thrives at excessively high light intensities by exceptionally enhancing the mechanisms that protect photosynthesis from photoinhibition. Plant J. 2021 doi: 10.1111/tpj.15232. PubMed DOI

Treves H., Raanan H., Kedem I., Murik O., Keren N., Zer H., Berkowicz S.M., Giordano M., Norici A., Shotland Y., et al. The mechanisms whereby the green alga Chlorella ohadii, isolated from desert soil crust, exhibits unparalleled photodamage resistance. New Phytol. 2016 doi: 10.1111/nph.13870. PubMed DOI

Treves H., Raanan H., Finkel O.M., Berkowicz S.M., Keren N., Shotland Y., Kaplan A. A newly isolated Chlorella sp. from desert sand crusts exhibits a unique resistance to excess light intensity. FEMS Microbiol. Ecol. 2013;86:373–380. doi: 10.1111/1574-6941.12162. PubMed DOI

Hemme D., Veyel D., Muhlhaus T., Sommer F., Juppner J., Unger A.K., Sandmann M., Fehrle I., Schonfelder S., Steup M., et al. Systems-wide analysis of acclimation responses to long-term heat stress and recovery in the photosynthetic model organism Chlamydomonas reinhardtii. Plant Cell. 2014;26:4270–4297. doi: 10.1105/tpc.114.130997. PubMed DOI PMC

Semenenko V.E., Vladimirova M.G., Orleanskaya O.B. Physiological characteristics of Chlorella sp. K under conditions of high extremal temperatures I. Uncoupling effect of extreme temperatures on the cellular functions of Chlorella. Russian J. Plant Physiol. 1967;14:612–625.

Zachleder V., Brányiková I. Starch overproduction by means of algae. In: Bajpai R.K., Prokop A., Zappi M., editors. Algal biorefineries. 1: Cultivation of cells and products. Springer; Dordrecht, The Netherlands: Heidelberg, Germany: London, UK: New York, NY, USA: 2014. pp. 217–240.

Cedergreen N., Streibig J.C., Kudsk P., Mathiassen S.K., Duke S.O. The occurrence of hormesis in plants and algae. Dose Response. 2006;5:150–162. doi: 10.2203/dose-response.06-008.Cedergreen. PubMed DOI PMC

Calabrese E.J., Mattson M.P. How does hormesis impact biology, toxicology, and medicine? NPJ Aging Mech. Dis. 2017;3:13. doi: 10.1038/s41514-017-0013-z. PubMed DOI PMC

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