Growth under Different Trophic Regimes and Synchronization of the Red Microalga Galdieria sulphuraria

. 2021 Jun 24 ; 11 (7) : . [epub] 20210624

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34202768

The extremophilic unicellular red microalga Galdieria sulphuraria (Cyanidiophyceae) is able to grow autotrophically, or mixo- and heterotrophically with 1% glycerol as a carbon source. The alga divides by multiple fission into more than two cells within one cell cycle. The optimal conditions of light, temperature and pH (500 µmol photons m-2 s-1, 40 °C, and pH 3; respectively) for the strain Galdieria sulphuraria (Galdieri) Merola 002 were determined as a basis for synchronization experiments. For synchronization, the specific light/dark cycle, 16/8 h was identified as the precondition for investigating the cell cycle. The alga was successfully synchronized and the cell cycle was evaluated. G. sulphuraria attained two commitment points with midpoints at 10 and 13 h of the cell cycle, leading to two nuclear divisions, followed subsequently by division into four daughter cells. The daughter cells stayed in the mother cell wall until the beginning of the next light phase, when they were released. Accumulation of glycogen throughout the cell cycle was also described. The findings presented here bring a new contribution to our general understanding of the cell cycle in cyanidialean red algae, and specifically of the biotechnologically important species G. sulphuraria.

Zobrazit více v PubMed

Merola A., Castaldo R., De Luca P., Gambardella R., Musacchio A., Taddei R. Revision of Cyanidium caldarium. Three species of acidophilic algae. Plant Biosyst. 1981;115:189–195. doi: 10.1080/11263508109428026. DOI

Matsuzaki M., Misumi O., Shin-i T., Maruyama S., Takahara M., Miyagishima S., Mori T., Nishida K., Yagisawa F., Nishida K., et al. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature. 2004;428:653–657. doi: 10.1038/nature02398. PubMed DOI

Schonknecht G., Chen W.H., Ternes C.M., Barbier G.G., Shrestha R.P., Stanke M., Brautigam A., Baker B.J., Banfield J.F., Garavito R.M., et al. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science. 2013;339:1207–1210. doi: 10.1126/science.1231707. PubMed DOI

Qiu H., Price D.C., Weber A.P., Reeb V., Yang E.C., Lee J.M., Kim S.Y., Yoon H.S., Bhattacharya D. Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea. Curr. Biol. 2013;23:865–866. doi: 10.1016/j.cub.2013.08.046. PubMed DOI

Rossoni A.W., Price D.C., Seger M., Lyska D., Lammers P., Bhattacharya D., Weber A.P.M. The genomes of polyextremophilic cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions. eLife. 2019;8 doi: 10.7554/eLife.45017. PubMed DOI PMC

De Luca P., Taddei R., Varano L. Cyanidioschyzon merolae: A new alga of thermal acidic environments. Webbia. 1978;33:37–44. doi: 10.1080/00837792.1978.10670110. DOI

Seckbach J. Evolutionary Pathways and Enigmatic Algae: Cyanidium Caldarium (Rhodophyta) and Related Cells. Kluwer Academic Publisher; Dordrecht, The Netherlands: 1994.

Gross W., Küver J., Tischendorf G., Bouchaala N., Büsch W. Cryptoendolithic growth of the red alga Galdieria sulphuraria in volcanic areas. Eur. J. Phycol. 1998;33:25–31. doi: 10.1080/09670269810001736503. DOI

Ciniglia C., Yoon H.S., Pollio A., Pinto G., Bhattacharya D. Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol. Ecol. 2004;13:1827–1838. doi: 10.1111/j.1365-294X.2004.02180.x. PubMed DOI

Reeb V., Bhattacharya D. Red Algae in the Genomic Age. Volume 13. Springer; Dordrecht, The Netherlands: 2010. The Thermo-Acidophilic Cyanidiophyceae (Cyanidiales) pp. 409–426. Cellular Origin, Life in Extreme Habitats and Astrobiology. DOI

Vítová M., Goecke F., Sigler K., Řezanka T. Lipidomic analysis of the extremophilic red alga Galdieria sulphuraria in response to changes in pH. Algal Res. 2016;13:218–226. doi: 10.1016/j.algal.2015.12.005. DOI

Hirooka S., Tomita R., Fujiwara T., Ohnuma M., Kuroiwa H., Kuroiwa T., Miyagishima S. Efficient open cultivation of cyanidialean red algae in acidified seawater. Sci. Rep. 2020;10:1–12. doi: 10.1038/s41598-020-70398-z. PubMed DOI PMC

Yoshimura E., Nagasaka S., Sato Y., Satake K., Mori S. Extraordinary high aluminium tolerance of the acidophilic thermophilic alga, Cyanidium caldarium. Soil Sci. Plant. Nutr. 1999;45:721–724. doi: 10.1080/00380768.1999.10415835. DOI

Nagasaka S., Nishizawa N.K., Watanabe T., Mori S., Yoshimura E. Evidence that electron-dense bodies in Cyanidium caldarium have an iron-storage role. Biometals. 2003;16:465–470. doi: 10.1023/A:1022563600525. PubMed DOI

Minoda A., Sawada H., Suzuki S., Miyashita S., Inagaki K., Yamamoto T., Tsuzuki M. Recovery of rare earth elements from the sulfothermophilic red alga Galdieria sulphuraria using aqueous acid. Appl. Microbiol. Biotechnol. 2015;99:1513–1519. doi: 10.1007/s00253-014-6070-3. PubMed DOI

Cizkova M., Mezricky P., Mezricky D., Rucki M., Zachleder V., Vitova M. Bioaccumulation of rare earth elements from waste luminophores in the red algae, Galdieria phlegrea. Waste Biomass Valor. 2020 doi: 10.1007/s12649-020-01182-3. DOI

Čížková M., Vítová M., Zachleder V. The Red Microalga Galdieria as a Promising Organisms for Applications in Biotechnolgy. In: Vítová M., editor. Microalgae. From Physiology to Application. IntechOpen; London, UK: 2020. pp. 1–17.

Varshney P., Mikulic P., Vonshak A., Beardall J., Wangikar P.P. Extremophilic micro-algae and their potential contribution in biotechnology. Biores. Technol. 2015;184:363–372. doi: 10.1016/j.biortech.2014.11.040. PubMed DOI

Ju X., Igarashi K., Miyashita S., Mitsuhashi H., Inagaki K., Fujii S., Sawada H., Kuwabara T., Minoda A. Effective and selective recovery of gold and palladium ions from metal wastewater using a sulfothermophilic red alga, Galdieria sulphuraria. Biores. Technol. 2016;211:759–764. doi: 10.1016/j.biortech.2016.01.061. PubMed DOI

Gross W., Schnarrenberger C. Heterotrophic growth of two strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol. 1995;36:633–638.

Oesterhelt C., Schnarrenberger C., Gross W. Characterization of a sugar/polyol uptake system in the red alga Galdieria sulphuraria. Eur. J. Phycol. 1999;34:271–277. doi: 10.1080/09670269910001736322. DOI

Oesterhelt C., Schmalzlin E., Schmitt J.M., Lokstein H. Regulation of photosynthesis in the unicellular acidophilic red alga Galdieria sulphuraria. Plant J. 2007;51:500–511. doi: 10.1111/j.1365-313X.2007.03159.x. PubMed DOI

Lopez G., Yate C., Ramos F.A., Cala M.P., Restrepo S., Baena S. Production of polyunsaturated fatty acids and lipids from autotrophic, mixotrophic and heterotrophic cultivation of Galdieria sp. strain USBA-GBX-832. Sci. Rep. 2019;9 doi: 10.1038/s41598-019-46645-3. PubMed DOI PMC

Li C., Lesnik K.L., Liu H. Conversion of waste glycerol from biodiesel production into value-added products. Energies. 2013;6:4739–4768. doi: 10.3390/en6094739. DOI

Xu S., Elsayed M., Ismail G.A., Li C., Wang S., El-Fatah Abomohra A. Evaluation of bioethanol and biodiesel production from Scenedesmus obliquus grown in biodiesel waste glycerol: A sequential integrated route for enhanced energy recovery. Energy Convers. Manag. 2019;197:111907. doi: 10.1016/j.enconman.2019.111907. DOI

Martinez-Garcia M., Kormpa A., van der Maarel M.J.E.C. The glycogen of Galdieria sulphuraria as alternative to starch for the production of slowly digestible and resistant glucose polymers. Carbohydr. Polym. 2017;169:75–82. doi: 10.1016/j.carbpol.2017.04.004. PubMed DOI

Martinez-Garcia M., Stuart M.C.A., van der Maarel M.J.E. Characterization of the highly branched glycogen from the thermoacidophilic red microalga Galdieria sulphuraria and comparison with other glycogens. Int. J. Biol. Macromol. 2016;89:12–18. doi: 10.1016/j.ijbiomac.2016.04.051. PubMed DOI

John P.C.L. Control of the cell division cycle in Chlamydomonas. Microbiol. Sci. 1984;1:96–101. PubMed

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

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

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. 1975;14:70–104.

Donnan L., Carvill E.P., Gilliland T.J., John P.C.L. The cell-cycles of Chlamydomonas and Chlorella. N. Phytol. 1985;99:1–40. doi: 10.1111/j.1469-8137.1985.tb03634.x. 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

Vítová M., Zachleder V. Points of commitment to reproductive events as a tool for analysis of the cell cycle in synchronous cultures of algae. Folia Microbiol. 2005;50:141–149. doi: 10.1007/BF02931463. PubMed DOI

Calhoun S., Bell T.A.S., Dahlin L.R., Kunde Y., LaButti K., Louie K.B., Kuftin A., Treen D., Dilworth D., Mihaltcheva S., et al. A multi-omic characterization of temperature stress in a halotolerant Scenedesmus strain for algal biotechnology. Commun. Biol. 2021;4 doi: 10.1038/s42003-021-01859-y. PubMed DOI PMC

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

Zachleder V., Ivanov I., Vitova M., Bisova K. Cell cycle arrest by supraoptimal temperature in the alga Chlamydomonas reinhardtii. Cells. 2019;8:1237. doi: 10.3390/cells8101237. 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. Physiol. Plants. 1967;14:612–625.

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

Selvaratnam T., Pegallapati A.K., Montelya F., Rodriguez G., Nirmalakhandan N., Van Voorhies W., Lammers P.J. Evaluation of a thermo-tolerant acidophilic alga, Galdieria sulphuraria, for nutrient removal from urban wastewaters. Biores. Technol. 2014;156:395–399. doi: 10.1016/j.biortech.2014.01.075. PubMed DOI

Albertano P., Ciniglia C., Pinto G., Pollio A. The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: An update. Hydrobiologia. 2000;433:137–143. doi: 10.1023/A:1004031123806. DOI

Jong L.W., Fujiwara T., Hirooka S., Miyagishima S.Y. Cell size for commitment to cell division and number of successive cell divisions in cyanidialean red algae. Protoplasma. 2021 doi: 10.1007/s00709-021-01628-y. PubMed DOI

Bišová 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

Zachleder V., Bišová K., Vítová M. The Cell Cycle of Microalgae. In: Borowitzka M.A., Raven J.A., editors. The Physiology of Microalgae. 6th ed. Springer International Publishing Switzerland; Cham, Switzerland: 2016. pp. 3–46.

Reed S.I. The selection of S. cerevisiae mutants defective in the start event of cell division. Genetics. 1980;95:561–577. doi: 10.1093/genetics/95.3.561. PubMed DOI PMC

Pardee A.B. A restriction point for control of normal animal cell proliferation. Proc. Nat. Acad. Sci. USA. 1974;71:1286–1290. doi: 10.1073/pnas.71.4.1286. PubMed DOI PMC

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

Reinecke D.L., Castillo-Flores A., Boussiba S., Zarka A. Polyploid polynuclear consecutive cell-cycle enables large genome-size in Haematococcus pluvialis. Algal Res. Biomass Biofuels Bioprod. 2018;33:456–461. doi: 10.1016/j.algal.2018.06.013. DOI

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

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., Walker J.M., editors. Plant Cell Division. Springer Science; New York, NY, USA: 2016. pp. 3–16. Methods in Molecular Biology. PubMed

Miyagishima S.Y., Fujiwara T., Sumiya N., Hirooka S., Nakano A., Kabeya Y., Nakamura M. Translation-independent circadian control of the cell cycle in a unicellular photosynthetic eukaryote. Nat. Commun. 2014;5:3807. doi: 10.1038/ncomms4807. PubMed DOI

Imoto Y., Fujiwara T., Yoshida Y., Kuroiwa H., Maruyama S., Kuroiwa T. Division of cell nuclei, mitochondria, plastids, and microbodies mediated by mitotic spindle poles in the primitive red alga Cyanidioschyzon merolae. Protoplasma. 2010;241:63–74. doi: 10.1007/s00709-010-0107-y. PubMed DOI

Moriyama T., Terasawa K., Sekine K., Toyoshima M., Koike M., Fujiwara M., Sato N. Characterization of cell-cycle-driven and light-driven gene expression in a synchronous culture system in the unicellular rhodophyte Cyanidioschyzon merolae. Microbiol. Sgm. 2010;156:1730–1737. doi: 10.1099/mic.0.037754-0. PubMed DOI

Kanesaki Y., Imamura S., Minoda A., Tanaka K. External light conditions and internal cell cycle phases coordinate accumulation of chloroplast and mitochondrial transcripts in the red alga Cyanidioschyzon merolae. DNA Res. 2012;19:289–303. doi: 10.1093/dnares/dss013. PubMed DOI PMC

Sumiya N., Fujiwara T., Era A., Miyagishima S. Chloroplast division checkpoint in eukaryotic algae. Proc. NatL. Acad. Sci. USA. 2016;113:7629–7638. doi: 10.1073/pnas.1612872113. PubMed DOI PMC

Fujiwara T., Hirooka S., Ohbayashi R., Onuma R., Miyagishima S.Y. Relationship between cell cycle and diel transcriptomic changes in metabolism in a unicellular red alga. Plant Physiol. 2020;183:1484–1501. doi: 10.1104/pp.20.00469. PubMed DOI PMC

Ichinose T.M., Iwane A.H. Long-term live cell cycle imaging of single Cyanidioschyzon merolae cells. Protoplasma. 2021;258:651–660. doi: 10.1007/s00709-020-01592-z. PubMed DOI PMC

Sheath R.G., Hellebust J.A., Sawa T. Floridean starch metabolism of Porphyridium purpureum (Rhodphyta) II Changes during the cell cycle. Phycologia. 1979;18:185–190. doi: 10.2216/i0031-8884-18-3-185.1. DOI

Simon-Bercovitch B., Bar-Zvi D., Arad S.M. Cell-wall formation during the cell cycle of Porphyridium sp. (Rhodophyta) J. Phycol. 1999;35:78–83. doi: 10.1046/j.1529-8817.1999.3510078.x. DOI

Knappe J. Synchronkulturen von Porphyridium cruentum und ihr photosynthetisches Verhalten. Plant Biol. 1972;85:425–434. doi: 10.1111/j.1438-8677.1972.tb04143.x. DOI

Kopecky J., Lukavska A., Verbovikova E., Pfuendel E. Changes in the photosynthetic pigment patterns during the synchronous life cycle of Porphyridium purpureum. Arch. Hydrobiol. Suppl. 2004;154:121–132. doi: 10.1127/1864-1318/2004/0114-0121. DOI

Rebolloso Fuentes M.M., García Sánchez J.L., Fernández Sevilla J.M., Acién Fernández F.G., Sánchez Pérez J.A., Molina Grima E. Outdoor continuous culture of Porphyridium cruentum in a tubular photobioreactor: Quantitative analysis of the daily cyclic variation of culture parameters. J. Biotechnol. 1999;70:271–288. doi: 10.1016/S0168-1656(99)00080-2. 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

Šetlík I., Zachleder V. The Multiple Fission Cell Reproductive Patterns in Algae. In: Nurse P., Streiblová E., editors. The Microbial Cell Cycle. CRC Press Inc.; Boca Raton, FL, USA: 1984. pp. 253–279.

Zachleder V., Cepák V. Visualization of DNA containing structures by fluorochrome DAPI in those algal cells which are not freely permeable to the dye. Arch. Hydrobiol. Algol. Stud. 1987;47:157–168.

Vítová M., Hendrychová J., Cepák V., Zachleder V. Visualization of DNA-containing structures in vivo in various species of Chlorophyta, Rhodophyta and Cyanophyta using SYBR Green I dye. Folia Microbiol. 2005;50:333–340. doi: 10.1007/BF02931414. PubMed 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. 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. 1984;67:313–328. doi: 10.1127/algol_stud/67/1984/313. DOI

Lowry O.H., Rosenbrough N.S., Farr A.L., Randall R.J. Protein measurement with the folin-phenol reagent. J. Biol. Chem. 1951;193:265–275. doi: 10.1016/S0021-9258(19)52451-6. PubMed DOI

Pinto G., Ciniglia C., Cascone C., Pollio A. Algae and Cyanobacteria in Extreme Environments. Volume 11. Springer; Dordrecht, The Netherlands: 2007. Species Composition of Cyanidiales Assemblages in Pisciarelli (Campi Flegrei, Italy) and Description of Galdieria Phlegrea sp. NOV; pp. 489–502. Cellular Origin, Life in Extreme Habitats and Astrobiology.

Eren A., Iovinella M., Yoon H.S., Cennamo P., de Stefano M., de Castro O., Ciniglia C. Genetic structure of Galdieria populations from Iceland. Polar Biol. 2018;41:1681–1691. doi: 10.1007/s00300-018-2308-3. DOI

Ciniglia C., Yang E.C., Pollio A., Pinto G., Iovinella M., Vitale L., Yoon H.S. Cyanidiophyceae in Iceland: Plastid rbcL gene elucidates origin and dispersal of extremophilic Galdieria sulphuraria and G. maxima (Galdieriaceae, Rhodophyta) Phycologia. 2014;53:542–551. doi: 10.2216/14-032.1. DOI

Gross W., Oesterhelt C., Tischendorf G., Lederer F. Characterization of a non-thermophilic strain of the red algal genus Galdieria isolated from SOOS (Czech Republic) Eur. J. Phycol. 2002;37:477–482. doi: 10.1017/S0967026202003773. DOI

Thangaraj B., Jolley C.C., Sarrou I., Bultema J.B., Greyslak J., Whitelegge J.P., Lin S., Kouril R., Subramanyam R., Boekema E.J., et al. Efficient Light Harvesting in a Dark, Hot, Acidic environment: The structure and function of PSI-LHCI from Galdieria sulphuraria. Biophys. J. 2011;100:135–143. doi: 10.1016/j.bpj.2010.09.069. PubMed DOI PMC

Liu L., Sanchez-Arcos C., Pohnert G., Wei D. Untargeted metabolomics unveil changes in autotrophic and mixotrophic Galdieria sulphuraria exposed to high-light intensity. Int. J. Mol. Sci. 2021;22:1247. doi: 10.3390/ijms22031247. PubMed DOI PMC

Curien G., Lyska D., Guglielmino E., Westhoff P., Janetzko J., Tardif M., Hallopeau C., Brugiere S., Dal Bo D., Decelle J., et al. Mixotrophic growth of the extremophile Galdieria sulphuraria reveals the flexibility of its carbon assimilation metabolism. N. Phytol. 2021;231:326–338. doi: 10.1111/nph.17359. PubMed DOI PMC

Kuroiwa T., Nagashima H., Fukuda I. Chloroplast division without DNA synthesis during the life cycle of the unicellular alga Cyanidium caldarium M-8 as revealed by quantitative fluorescence microscopy. Protoplasma. 1989;149:120–129. doi: 10.1007/BF01322984. 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

Ball S., Colleoni C., Cenci U., Raj J.N., Tirtiaux C. The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J. Exp. Bot. 2011;62:1775–1801. doi: 10.1093/jxb/erq411. PubMed DOI

Sakurai T., Aoki M., Ju X., Ueda T., Nakamura Y., Fujiwara S., Umemura T., Tsuzuki M., Minoda A. Profiling of lipid and glycogen accumulations under different growth conditions in the sulfothermophilic red alga Galdieria sulphuraria. Biores. Technol. 2016;200:861–866. doi: 10.1016/j.biortech.2015.11.014. PubMed DOI

Salbitani G., Cipolletta S., Vona V., Di Martino C., Carfagna S. Heterotrophic cultures of Galdieria phlegrea shift to autotrophy in the presence or absence of glycerol. J. Plant Growth Regul. 2021;40:371–378. doi: 10.1007/s00344-020-10109-0. DOI

Carbone D.A., Olivieri G., Pollio A., Melkonian M. Comparison of Galdieria growth and photosynthetic activity in different culture systems. AMB Express. 2020;10:170. doi: 10.1186/s13568-020-01110-7. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace