Supra-Optimal Temperature: An Efficient Approach for Overaccumulation of Starch in the Green Alga Parachlorella kessleri
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
17-06264S
Grantová Agentura České Republiky
AVOZ61388971
Institutional Research Concept
PubMed
34359975
PubMed Central
PMC8306380
DOI
10.3390/cells10071806
PII: cells10071806
Knihovny.cz E-zdroje
- Klíčová slova
- Parachlorella kessleri, cell cycle, deuterated lipid, deuterated starch, deuterium, energy reserves, growth processes, microalgae, reproduction events, starch, supra-optimal temperature,
- MeSH
- biomasa MeSH
- buněčné dělení fyziologie MeSH
- Chlorophyta růst a vývoj MeSH
- lipidy MeSH
- metabolismus lipidů fyziologie MeSH
- mikrořasy metabolismus MeSH
- škrob metabolismus MeSH
- teplota * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- lipidy MeSH
- škrob MeSH
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.
Faculty of Science University of South Bohemia 37005 České Budějovice Czech Republic
The University of Tokyo Future Center Initiative Wakashiba 178 4 4 Kashiwa 277 0871 Chiba Japan
Zobrazit více v PubMed
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
The Effect of Variable Light Source and Light Intensity on the Growth of Three Algal Species