Генетическая инженерия в биотехнологии микроводорослей: достижения и перспективы
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Аннотация
В данном обзоре обобщается информация о применении методов генной инженерии для модификации диатомовых и зелёных микроводорослей с целью получения штаммов с улучшенными или заданными признаками. Рассматриваются кратко основные методы, достигнутые результаты и перспективы использования генетически модифицированных штаммов микроводорослей в биотехнологии. Представлены успешные примеры применения методов направленного редактирования генома для модификации модельных видов микроводорослей Chlamydomonas reinhardtii P.A.Dangeard, 1888 и Phaeodactylum tricornutum Bohlin, 1897. Показано, что нокауты и оверэкспрессия ключевых генов позволяют значительно увеличивать накопление липидов в биомассе водорослей без существенного влияния на рост, демонстрируя перспективность данного подхода в оптимизации биотехнологического потенциала штаммов.
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Библиографические ссылки
A Look Back at the U.S. Department of Energy’s Aquatic Species Program: Biodiesel from Algae : NREL/TR-580-24190 / Sheehan J., Dunahay T., Benemann J., Roessler P. ; Nat. Renewable Energy Lab. – Golden, USA : NREL, 1998. – 294 p.
Adem M., Beyene D., Feyissa T. Recent achievements obtained by chloroplast transformation // Plant Methods. – 2017. – Vol. 13. – Art. 30. – URL: https://plantmethods.biomedcentral.com/ articles/10.1186/s13007-017-0179-1. – Publ. date: 19.04.2017.
Ambati R. R., Gogisetty D., Aswathanarayana R. G., Ravi S., Bikkina P. N., Bo L., Yuepeng S. Industrial potential of carotenoid pigments from microalgae: current trends and future prospects // Critical Reviews in Food Science and Nutrition. – 2019. – Vol. 59, iss. 12. – P. 1880–1902. – https://doi.org/10.1080/10408398.2018.1432561
Andrianantoandro E., Basu S., Karig D., Weiss R. Synthetic biology: new engineering rules for an emerging discipline // Molecular Systems Biology. – 2006. – Vol. 2. – Art. 28. – URL: https://www.embopress.org/doi/full/10.1038/msb4100073. – Publ. date: 16.05.2006.
Anila N., Simon D. P., Chandrashekar A., Ravishankar G. A., Sarada R. Metabolic engineering of Dunaliella salina for production of ketocarotenoids // Photosynthesis research. – 2016. – Vol. 127, iss. 3. – P. 321–333. – https://doi.org/10.1007/s11120-015-0188-8
Apt K. E., Grossman A. R., Kroth-Pancic P. G. Stable nuclear transformation of the diatom Phaeodactylum tricornutum // Molecular and General Genetics. – 1996. – Vol. 252, iss. 5. – P. 572–579. – https://doi.org/10.1007/BF02172403
Basheer S., Huo S., Zhu F., Qian J., Xu L., Cui F., Zou B. Microalgae in human health and medicine // Microalgae Biotechnology for Food, Health and High Value Products / eds by M. A. Alam [et al.]. – Singapore : Springer, 2020. – Chap. 5. – P. 149–174.
Bo Y., Wang K., Wu Y., Cao H., Cui Y., Wang L. Establishment of a chloroplast transformation system in Tisochrysis lutea // Journal of Applied Phycology. – 2020. – Vol. 32, iss. 5. – P. 2959–2965. – https://doi.org/10.1007/s10811-020-02159-4
Boynton J. E., Gillham N. W., Harris E. H., Hosler J. P., Johnson A. M., Jones A. R., RandolphAnderson B. L., Robertson D., Klein T. M., Shark K. B., Sanford J. C. Chloroplast transformation in Chlamydomonas with high velocity microprojectiles // Science. – 1988. – Vol. 240, iss. 4858. – P. 1534–1538. – https://doi.org/10.1126/science.2897716
Brennan L., Owende P. Biofuels from microalgae — a review of technologies for production, processing, and extractions of biofuels and co-products // Renewable and Sustainable Energy Reviews. – 2010. – Vol. 14, iss. 2. – P. 557–577. – https://doi.org/10.1016/j.rser.2009.10.009
Calder P. C. Very long-chain n-3 fatty acids and human health: fact, fiction and the future // Proceedings of the Nutrition Society. – 2018. – Vol. 77, iss. 1. – P. 52–72. – https://doi.org/10.1017/S0029665117003950
Cao K., Cui Y., Sun F., Zhang H., Fan J., Ge B., Cao Y., Wang X., Zhu X., Wei Z., Yao Q., Ma J., Wang Y., Meng C, Gao Z. Metabolic engineering and synthetic biology strategies for producing highvalue natural pigments in Microalgae // Biotechnology Advances. – 2023. – Vol. 68. – Art. 108236. – https://doi.org/10.1016/j.biotechadv.2023.108236
Carthew R. W., Sontheimer E. J. Origins and mechanisms of miRNAs and siRNAs // Cell. – 2009. – Vol. 136, iss. 4. – P. 642–655. – https://doi.org/10.1016/j.cell.2009.01.035
Cerutti H., Casas-Mollano J. A. On the origin and functions of RNA-mediated silencing: from protists to man // Current Genetics. – 2006. – Vol. 50, iss. 2. – P. 81–99. – https://doi.org/10.1007/s00294-006-0078-x
Cerutti H., Ma X., Msanne J., Repas T. RNA-mediated silencing in algae: biological roles and tools for analysis of gene function // Eukaryotic cell. – 2011. – Vol. 10, iss. 9. – P. 1164–1172. – https://doi.org/10.1128/EC.05106-11
Charoonnart P., Purton S., Saksmerprome V. Applications of microalgal biotechnology for disease control in aquaculture // Biology. – 2018. – Vol. 7, iss. 2. – P. 24. – https://doi.org/10.3390/biology7020024
Christian M., Cermak T., Doyle E. L., Schmidt C., Zhang F., Hummel A., Bogdanove A. J., Voytas D. F. Targeting DNA double-strand breaks with TAL effector nucleases // Genetics. – 2010. – Vol. 186, iss. 2. – P. 757–761. – https://doi.org/10.1534/genetics.110.120717
Coll J. M. Methodologies for transferring DNA into eukaryotic microalgae: a review // Spanish Journal of Agricultural Research. – 2006. – Vol. 4, iss. 4. – P. 316–330.
Couso I., Vila M., Rodriguez H., Vargas M. A., León R. Overexpression of an exogenous phytoene synthase gene in the unicellular alga Chlamydomonas reinhardtii leads to an increase in the content of carotenoids // Biotechnology progress. – 2011. – Vol. 27, iss. 1. – P. 54–60. – https://doi.org/10.1002/btpr.527
D’Adamo S., Schiano di Visconte G., Lowe G., Szaub-Newton J., Beacham T., Landels A., Allen M. J., Spicer A., Matthijs M. Engineering the unicellular alga Phaeodactylum tricornutum for high-value plant triterpenoid production // Plant Biotechnology Journal. – 2019. – Vol. 17, iss. 1. – P. 75–87. – https://doi.org/10.1111/pbi.12948
Daboussi F., Leduc S., Maréchal A., Dubois G., Guyot V., Perez-Michaut C., Amato A., Falciatore A., Juillerat A., Beurdeley M., Voytas D. F., Cavarec L., Duchateau P. Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology // Nature Communications. – 2014. – Vol. 5. – Art. 3831. – https://doi.org/10.1038/ncomms4831
Day A., Goldschmidt-Clermont M. The chloroplast transformation toolbox: selectable markers and marker removal // Plant Biotechnology Journal. – 2011. – Vol. 9, iss. 5. – P. 540–553. – https://doi.org/10.1111/j.1467-7652.2011.00604.x
De Riso V., Raniello R., Maumus F., Rogato A., Bowler C., Falciatore A. Gene silencing in the marine diatom Phaeodactylum tricornutum // Nucleic Acids Research. – 2009. – Vol. 37, iss. 14. – P. e96. – https://doi.org/10.1093/nar/gkp448
Debuchy R., Purton S., Rochaix J. D.Theargininosuccinatelyasegeneof Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus // EMBO Journal. – 1989. – Vol. 8, iss. 10. – P. 2803–2809. – https://doi.org/10.1002/j.1460-2075.1989.tb08426.x
Deng X., Cai J., Fei X. Effect of the expression and knock-down of citrate synthase gene on carbon flux during triacylglycerol biosynthesis by green algae Chlamydomonas reinhardtii // BMC Biochemistry. – 2013. – Vol. 14. – Art. 38. – https://doi.org/10.1186/1471-2091-14-38
Deng X., Cai J., Li Y., Fei X. Expression and knockdown of the PEPC1 gene affect carbon flux in the biosynthesis of triacylglycerols by the green alga Chlamydomonas reinhardtii // Biotechnology Letters. – 2014. – Vol. 36, iss. 11. – P. 2199–2208. – https://doi.org/10.1007/s10529-014-1593-3
Deng X. D., Gu B., Li Y. J., Hu X. W., Guo J. C., Fei X. W. The roles of acyl-CoA: diacylglycerol acyltransferase 2 genes in the biosynthesis of triacylglycerols by the green algae Chlamydomonas reinhardtii // Molecular Plant. – 2012. – Vol. 5, iss. 4. – P. 945–947. – https://doi.org/10.1093/mp/sss040
Diao J., Song X., Zhang L., Cui J., Chen L., Zhang W. Tailoring cyanobacteria as a new platform for highly efficient synthesis of astaxanthin // Metabolic Engineering. – 2020. – Vol. 61. – P. 275–287. – https://doi.org/10.1016/j.ymben.2020.07.003
Eilers U., Bikoulis A., Breitenbach J., Büchel C., Sandmann G. Limitations in the biosynthesis of fucoxanthin as targets for genetic engineering in Phaeodactylum tricornutum // Journal of applied phycology. – 2016. – Vol. 28, iss.1. – P. 123–129. – https://doi.org/10.1007/s10811-015-0583-8
Fabris M., George J., Kuzhiumparambil U., Lawson C. A., Jaramillo-Madrid A. C., Abbriano R. M., Vickers C. E., Ralph P. Extrachromosomal genetic engineering of the marine diatom Phaeodactylum tricornutum enables the heterologous production of monoterpenoids // ACS Synthetic Biology. – 2020. – Vol. 9, iss. 3. – P. 598–612. – https://doi.org/10.1021/acssynbio.9b00455
Fayyaz M., Chew K. W., Show P. L., Ling T. C., Ng I. S., Chang J. S. Genetic engineering of microalgae for enhanced biorefinery capabilities // Biotechnology advances. – 2020. – Vol. 43. – P. 107554. – https://doi.org/10.1016/j.biotechadv.2020.107554
Fire A., Xu S., Montgomery M. K., Kostas S. A., Driver S. E., Mello C. C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans // Nature. – 1998. – Vol. 391, iss. 6669. – P. 806−811. – https://doi.org/10.1038/35888
Fu W., Chaiboonchoe A., Khraiwesh B., Nelson D. R., Al-Khairy D., Mystikou A., Alzahmi A., Salehi- Ashtiani K. Algal cell factories: approaches, applications, and potentials // Marine Drugs. – 2016. – Vol. 14, iss. 12. – Art. 225. – https://doi.org/10.3390/md14120225
Gan Q., Jiang J., Han X., Wang S., Lu Y. Engineering the chloroplast genome of oleaginous marine microalga Nannochloropsis oceanica // Frontiers in Plant Science. – 2018. – Vol. 9. – P. 439. – https://doi.org/10.3389/fpls.2018.00439
Gao, X., Jing, X., Liu, X., Lindblad P. Biotechnological production of the sunscreen pigment scytonemin in cyanobacteria: progress and strategy // Marine Drugs. – 2021. – Vol. 19, iss. 3. – Art. 129. – https://doi.org/10.3390/md19030129
Gimpel J. A., Henríquez V., Mayfield S. P. In metabolic engineering of eukaryotic microalgae: potential and challenges come with great diversity // Frontiers in microbiology. – 2015. – Vol. 6. – Art. 1376. – https://doi.org/10.3389/fmicb.2015.01376
Goldschmidt-Clermont M. Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker of site-directed transformation of Chlamydomonas // Nucleic AcidsResearch.–1991.–Vol.19,iss.15.–P.4083–4089.–https://doi.org/10.1093/nar/19.15.4083
Goswami R. K., Agrawal K., Upadhyaya H. M., Gupta V. K., Verma P. Microalgae conversion to alternative energy, operating environment and economic footprint: an influential approach towards energy conversion, and management // Energy Conversion and Management. – 2022. – Vol. 269. – Art. 116118. – https://doi.org/10.1016/j.enconman.2022.116118
Greiner A., Kelterborn S., Evers H., Kreimer G., Sizova I., Hegemann P. Targeting of photoreceptor genes in Chlamydomonas reinhardtii via zinc-finger nucleases and CRISPR/Cas9 // Plant Cell. – 2017. – Vol. 29, iss. 10. – P. 2498–2518. – https://doi.org/10.1105/tpc.17.00659
Guo C., Anwar M., Mei R., Li X., Zhao D., Jiang Y., Zhuang J., Liu C., Wang C., Hu Z. Establishment and optimization of PEG-mediated protoplast transformation in the microalga Haematococcus pluvialis // Journal of Applied Phycology. – 2022. – Vol. 34, iss. 3. – P. 1595–1605. – https://doi.org/10.1007/s10811-022-02718-x
Gutiérrez S., Lauersen K. J. Gene delivery technologies with applications in microalgal genetic engineering // Biology. – 2021. – Vol. 10, iss. 4. – P. 265. – https://doi.org/10.3390/biology10040265
Harris E. H. Chlamydomonas as a model organism // Annual Review of Plant Physiology and Plant Molecular Biology. – 2001. – Vol. 52. – P. 363–406. – https://doi.org/10.1146/annurev.arplant.52.1.363
Hossain N., Hasan M. H., Mahlia T. M. I., Shamsuddin A. H., Silitonga A. S. Feasibility of microalgae as feedstock for alternative fuel in Malaysia: a review // Energy Strategy Reviews. – 2020. – Vol. 32. – Art. 100536. – https://doi.org/https://doi.org/10.1016/j.esr.2020.100536
Hsieh H. J., Su C. H., Chien L. J. Accumulation of lipid production in Chlorella minutissima by triacylglycerol biosynthesis-related genes cloned from Saccharomyces cerevisiae and Yarrowia lipolytica // Journal of Microbiology. – 2012. – Vol. 50, iss. 3. – P. 526–534. – https://doi.org/10.1007/s12275-012-2041-5
Hu J., Nagarajan D., Zhang Q., Chang J. S. Lee D. J. Heterotrophic cultivation of microalgae for pigment production: a review // Biotechnology Advances. – 2018. – Vol. 36, iss. 1. – P. 54–67. – https://doi.org/10.1016/j.biotechadv.2017.09.009
Hu L., Feng S., Liang G., Du J., Li A., Niu C. CRISPR/Cas9-induced β-carotene hydroxylase mutation in Dunaliella salina CCAP19/18 // AMB Express. – 2021. – Vol. 11. – Art. 83. – https://doi.org/10.1186/s13568-021-01242-4
Ibuot A., Webster R. E., Williams L. E., Pittman J. K. Increased metal tolerance and bioaccumulation of zinc and cadmium in Chlamydomonas reinhardtii expressing a AtHMA4 C‐terminal domain protein // Biotechnology and Bioengineering. – 2020. – Vol. 117, iss. 10. – P. 2996–3005. – https://doi.org/10.1002/bit.27476
Ishikura K., Takaoka Y., Kato K., Sekine M., Yoshida K., Shinmyo A. Expression of a foreign gene in Chlamydomonas reinhardtii chloroplast // Journal of Bioscience and Bioengineering. – 1999. – Vol. 87, iss. 3. – P. 307–314. – https://doi.org/10.1016/S1389-1723(99)80037-1
Jagadevan S., Banerjee A., Banerjee C., Guria C., Tiwari R., Baweja M., Shukla P. Recent developments in synthetic biology and metabolic engineering in microalgae towards biofuel production // Biotechnology for Biofuels. – 2018. – Vol. 11. – Art. 185. – https://doi.org/10.1186/s13068-018-1181-1
Jeong B. R., Jang J., Jin E. Genome engineering via gene editing technologies in microalgae // Bioresource Technology. – 2023. – Vol. 373. – Art. 128701. – https://doi.org/10.1016/j.biortech.2023.128701
Jia Y., Xue L., Liu H., Li J. Characterization of the glyceraldehyde-3-phosphate dehydrogenase (GAPDH) gene from the halotolerant alga Dunaliella salina and inhibition of its expression by RNAi // Current Microbiology. – 2009. – Vol. 58, iss. 5. – P. 426–431. – https://doi.org/10.1007/s00284008-9333-3
Jiang W., Brueggeman A. J., Horken K. M., Plucinak T. M., Weeks D. P. Successful transient expression of Cas9 and single guide RNA genes in Chlamydomonas reinhardtii // Eukaryotic Cell. – 2014. – Vol. 13, iss. 11. – P. 1465–1469. – https://doi.org/10.1128/EC.00213-14
Jiang W. Z., Weeks D. P. A gene-within-a-gene Cas9/sgRNA hybrid construct enables gene editing andgenereplacementstrategiesin Chlamydomonas reinhardtii //AlgalResearch.–2017.–Vol.26.– P. 474–480. – https://doi.org/10.1016/j.algal.2017.04.001
Kalra R., Gaur S., Goel M. Microalgae bioremediation: a perspective towards wastewater treatment along with industrial carotenoids production // Journal of Water Process Engineering. – 2021. – Vol. 40. – Art. 101794. – https://doi.org/10.1016/j.jwpe.2020.101794
Kao P.-H., Ng I-S. CRISPRi mediated phosphoenolpyruvate carboxylase regulation to enhance the production of lipid in Chlamydomonas reinhardtii // Bioresource Technology. – 2017. – Vol. 245, pt. B. – P. 1527–1537. – https://doi.org/10.1016/j.biortech.2017.04.111
Kathiresan S., Sarada R. Towards genetic improvement of commercially important microalga Haematococcus pluvialis for biotech applications // Journal of Applied Phycology. – 2009. – Vol. 21, iss. 5. – P. 553–558. – https://doi.org/10.1007/s10811-009-9414-0
Kato K., Marui T., Kasai S., Shinmyo A. Artificial control of transgene expression in Chlamydomonas reinhardtii chloroplast using the lac regulation system from Escherichia coli // Journal of Bioscience and Bioengineering. – 2007. – Vol. 104, iss. 3. – P. 207–213. – https://doi.org/10.1263/jbb.104.207
Kazamia E., Smith A. G. Assessing the environmental sustainability of biofuels // Trends in Plant Science. – 2014. – Vol. 19, iss. 10. – P. 615–618. – https://doi.org/10.1016/j.tplants.2014.08.001
Kholssi R., Lougraimzi H., Moreno-Garrido I. Effects of global environmental change on microalgal photosynthesis, growth and their distribution // Marine Environmental Research. – 2023. – Vol. 184. – Art. 105877. – https://doi.org/10.1016/j.marenvres.2023.105877
Kilian O., Benemann C. S. E., Niyogi K. K., Vick B. High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. // Proceedings of the National Academy of Sciences of the USA. – 2011. – Vol. 108, no. 52. – P. 21265–21269. – https://doi.org/10.1073/pnas.1105861108
Kim E.-J., Ma X., Cerutti H. Gene silencing in microalgae: mechanisms and biological roles // Bioresource Technology. – 2015. – Vol. 184. – P. 23–32. – https://doi.org/10.1016/j.biortech.2014.10.119
Kim Y. G., Cha J., Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain // Proceedings of the National Academy of Sciences of the USA. – 1996. – Vol. 93, no. 3. – P. 1156–1160. – https://doi.org/10.1073/pnas.93.3.1156
Kindle K. L., Schnell R. A., Fernandez E., Lefebvre P. A. Stable nuclear transformation of Chlamydomonas using the Chlamydomonas gene for nitrate reductase // Journal of Cell Biology. – 1989. – Vol. 109, iss. 6. – P. 2589–2601. – https://doi.org/10.1083/jcb.109.6.2589
Klievik B. J., Tyrrell A. D., Chen C. T., Bazinet R. P. Measuring brain docosahexaenoic acid turnover as a marker of metabolic consumption // Pharmacology & Therapeutics. – 2023. – Vol. 248. – Art. 108437. – https://doi.org/10.1016/j.pharmthera.2023.108437
Kong F., Yamaoka Y., Ohama T., Lee Y., Li-Beisson Y. Molecular genetic tools and emerging synthetic biology strategies to increase cellular oil content in Chlamydomonas reinhardtii // Plant and Cell Physiology. – 2019. – Vol. 60, iss. 6. – P. 1184–1196. – https://doi.org/10.1093/pcp/pcz022
Kroth P. G., Bones A. M., Daboussi F., Ferrante M. I., Jaubert M., Kolot M., Nymark M., Río Bártulos C., Ritter A., Russo M. T., Serif M., Winge P., Falciatore A. Genome editing in diatoms: achievements and goals // Plant Cell Reports. – 2018. – Vol. 37, iss. 10. – P. 1401–1408. – https://doi.org/10.1007/s00299-018-2334-1
Kumar A. U., Ling A. P. K. Gene introduction approaches in chloroplast transformation and its applications // Journal of Genetic Engineering and Biotechnology. – 2021. – Vol. 19, iss. 1. – Art. 148. – https://doi.org/10.1186/s43141-021-00255-7
Kumar S. V., Misquitta R. W., Reddy V. S., Rao B. J., Rajam M. V. Genetic transformation of the green alga — Chlamydomonas reinhardtii by Agrobacterium tumefaciens // Plant Science. – 2004. – Vol. 166, iss. 3. – P. 731–738. – https://doi.org/10.1016/j.plantsci.2003.11.012
Kurita T., Moroi K., Iwai M., Okazaki K., Shimizu S., Nomura S., Saito F., Maeda S., Takami A., Sakamoto A., Ohta H., Sakuma T., Yamamoto T. Efficient and multiplexable genome editing using Platinum TALENs in oleaginous microalga, Nannochloropsis oceanica NIES‐2145 // Genes to Cells. – 2020. – Vol. 25, iss. 10. – P. 695–702. – https://doi.org/10.1111/gtc.12805
León-Saiki G. M., Remmers I. M., Martens D. E., Lamers P. P., Wijffels R. H., van der Veen D. The role of starch as transient energy buffer in synchronized microalgal growth in Acutodesmus obliquus // Algal research. – 2017. – Vol. 25. – P. 160–167. – https://doi.org/10.1016/j.algal.2017.05.018
Liang M.-H., Wang L., Wang Q., Zhu J., Jiang J.-G. High-value bioproducts from microalgae: strategies and progress // Critical Reviews in Food Science and Nutrition. – 2019. – Vol. 59, iss. 15. – P. 2423–2441. – https://doi.org/10.1080/10408398.2018.1455030
Liang Z. C., Liang M. H., Jiang J. G. Transgenic microalgae as bioreactors // Critical Reviews in Food Science and Nutrition. – 2020. – Vol. 60, iss. 19. – P. 3195–3213. – https://doi.org/10.1080/10408398.2019.1680525
Liu J., Gerken H., Huang J., Chen F. Engineering of an endogenous phytoene desaturase gene as a dominant selectable marker for Chlamydomonas reinhardtii transformation and enhanced biosynthesis of carotenoids // Process Biochemistry. – 2013. – Vol. 48, iss. 5/6. – P. 788–795. – https://doi.org/10.1016/j.procbio.2013.04.020
Liu J., Sun Z., Gerken H., Huang J., Jiang Y., Chen F. Genetic engineering of the green alga Chlorella zofingiensis: a modified norflurazon-resistant phytoene desaturase gene as a dominant selectable marker // Applied Microbiology and Biotechnology. – 2014. – Vol. 98, iss. 11. – P. 5069–5079. – https://doi.org/10.1007/s00253-014-5593-y
Lumbreras V., Stevens D. R., Purton S. Efficient foreign gene expression in Chlamydomonas reinhardtii mediated by an endogenous intron // Plant Journal. – 1998. – Vol. 14, iss. 4. – P. 441–447. – https://doi.org/10.1046/j.1365-313X.1998.00145.x
Manuell A. L., Beligni M. V., Elder J. H., Siefker D. T., Tran M., Weber A., McDonald T. L., Mayfield S. P. Robust expression of a bioactive mammalian protein in Chlamydomonas chloroplast // Plant Biotechnology Journal. – 2007. – Vol. 5, iss. 3. – P. 402–412. – https://doi.org/10.1111/j.14677652.2007.00249.x
Mao X., Zhang Y., Wang X., Liu J. Novel insights into salinity-induced lipogenesis and carotenogenesis in the oleaginous astaxanthin-producing alga Chromochloris zofingiensis: a multi-omics study // Biotechnology for Biofuels. – 2020. – Vol. 13. – Art. 73. – https://doi.org/10.1186/s13068-020-01714-y
Mayfield S. P., Franklin S. E. Expression of human antibodies in eukaryotic microalgae // Vaccine. – 2005. – Vol. 23, iss. 15. – P. 1828–1832. – https://doi.org/10.1016/j.vaccine.2004.11.013
Meister G. Argonaute proteins: functional insights and emerging roles // Nature Reviews Genetics. – 2013. – Vol. 14, iss. 7. – P. 447–459. – https://doi.org/10.1038/nrg3462
Mishra A., Medhi K., Malaviya P., Thakur I. S. Omics approaches for microalgal applications: prospects and challenges // Bioresource Technology. – 2019. – Vol. 291. – Art. 121890. – https://doi.org/10.1016/j.biortech.2019.121890
Mitra M., Kirst H., Dewez D., Melis A. Modulation of the light-harvesting chlorophyll antenna size in Chlamydomonas reinhardtii by TLA1 gene over-expression and RNA interference // Philosophical Transactions of the Royal Society of London. Ser. B, Biological sciences. – 2012. – Vol. 367, nr 1608. – P. 3430–3443. – https://doi.org/10.1098/rstb.2012.0229
Moses T., Mehrshahi P., Smith A. G., Goossens A. Synthetic biology approaches for the production of plant metabolites in unicellular organisms // Journal of Experimental Botany. – 2017. – Vol. 68, no. 15. – P. 4057–4074. – https://doi.org/10.1093/jxb/erx119
Muñoz C. F., Südfeld C., Naduthodi M. I. S., Weusthuis R. A., Barbosa M. J., Wijffels R. H., D’Adamo S. Genetic engineering of microalgae for enhanced lipid production // Biotechnology Advances. – 2021. – Vol. 52. – Art. 107836. – https://doi.org/10.1016/j.biotechadv.2021.107836
Mussgnug J. H. Genetic tools and techniques for Chlamydomonas reinhardtii // Applied Microbiology and Biotechnology. – 2015. – Vol. 99, iss. 13. – P. 5407–5418. – https://doi.org/10.1007/s00253-015-6698-7
Ng S., Tan I., Kao H., Chang K., Chang S. Recent developments on genetic engineering of microalgae for biofuels and bio-based chemicals // Biotechnology Journal. – 2017. – Vol. 12, iss. 10. – Art. 1600644. – https://doi.org/10.1002/biot.201600644
Niu Y.-F., Yang Z.-K., Zhang M.-H., Zhu C.-C., Yang W.-D., Liu J.-S., Li H.-E. Transformation of diatom Phaeodactylum tricornutum by electroporation and establishment of inducible selection marker // Biotechniques. – 2012. – Vol. 52, iss. 6. – P. 1–3. – https://doi.org/10.2144/000113881
Nora L. C., Westmann C. A., Martins‐Santana L., Alves L. D., Monteiro L. M. O., Guazzaroni M.-E., Silva‐Rocha R. The art of vector engineering: towards the construction of next‐generation genetic tools // Microbial Biotechnology. – 2019. – Vol. 12, iss. 1. – P. 125–147. – https://doi.org/10.1111/1751-7915.13318
Novoveska L., Ross M. E., Stanley M. S., Pradelles R.,Wasiolek V., Sassi J. F. Microalgal carotenoids: a review of production, current markets, regulations, and future direction // Marine Drugs. – 2019. – Vol. 17, iss. 11. – Art. 640. – https://doi.org/10.3390/md17110640
Nymark M., Sharma A. K., Sparstad T., Bones A. M., Winge P. A CRISPR/Cas9 system adapted for gene editing in marine algae // Scientific Reports. – 2016. – Vol. 6. – Art. 24951. – https://doi.org/10.1038/srep24951
Occhialini A., Pfotenhauer A. C., Frazier T. P., Li L., Harbison S. A., Lail A. J., Mebane Z., Piatek A. A., Rigoulot S. B., Daniell H., Stewart C. N., Lenaghan S. C. Generation, analysis, and transformation of macro-chloroplast potato (Solanum tuberosum) lines for chloroplast biotechnology // Scientific Reports. – 2020. – Vol. 10. – Art. 21144. – https://doi.org/10.1038/s41598-020-78237-x
Oey M., Ross I. L., Stephens E., Steinbeck J., Wolf J., Radzun K. A., Kügler J., Ringsmuth A. K., Kruse O., Hankamer B. RNAi knock-down of LHCBM1, 2 and 3 increases photosynthetic H2 production efficiency of the green alga Chlamydomonas reinhardtii // PLoS ONE. – 2013. – Vol. 8, nr 4. – Art. e61375. – https://doi.org/10.1371/journal.pone.0061375
Ohnishi H., Saito Y. Eicosapentaenoic acid (EPA) reduces cardiovascular events: relationship with the EPA/arachidonic acid ratio // Journal of Atherosclerosis and Thrombosis. – 2013. – Vol. 20, iss. 12. – P. 861–877. – https://doi.org/10.5551/jat.18002
Patel A. K., Albarico F., Perumal P. K., Vadrale A. P., Nian C. T., Chau H. T. B., Anwar C., Wani H., Pal A., Saini R., Ha L. H., Senthilkumar B., Tsang Y.-S., Chen C.-W., Dong C.-D., Singhania R. R. Algae as an emerging source of bioactive pigments // Bioresource Technology. – 2022. – Vol. 351. – Art. 126910. – https://doi.org/10.1016/j.biortech.2022.126910
Perrine Z., Negi S., Sayre R. T. Optimization of photosynthetic light energy utilization by microalgae // Algal Research. – 2012. – Vol. 1, iss. 2. – P. 134–142. – https://doi.org/10.1016/j.algal.2012.07.002
Peter A. P., Koyande A. K., Chew K. W., Ho S. H., Chen W. H., Chang J. S., Krishnamoorthy R., Banat F., Show P. L. Continuous cultivation of microalgae in photobioreactors as a source of renewable energy: current status and future challenges // Renewable and Sustainable Energy Reviews. – 2022. – Vol. 154. – Art. 111852. – https://doi.org/10.1016/j.rser.2021.111852
Posewitz M. C., Smolinski S. L., Kanakagiri S., Melis A., Seibert M., Ghirardi M. L. Hydrogen photoproduction is attenuated by disruption of an isoamylase gene in Chlamydomonas reinhardtii // Plant Cell. – 2004. – Vol. 16, iss. 8. – P. 2151–2163. – https://doi.org/10.1105/tpc.104.021972
Ramazanov A., Ramazanov Z. Isolation and characterization of a starchless mutant of Chlorella pyrenoidosa STL-PI with a high growth rate, and high protein and polyunsaturated fatty acid content // Phycological Research. – 2006. – Vol. 54, iss. 4. – P. 255–259. – https://doi.org/10.1111/j.14401835.2006.00416.x
Ramesh V. M., Bingham S. E., Webber A. N. A simple method for chloroplast transformation in Chlamydomonas reinhardtii // Photosynthesis Research Protocols / ed. by Carpentier R. – 2nd ed. – New York [et al.] : Humana Press, 2011. – P. 313–320. – (Methods in molecular biology ; 684). – https://doi.org/10.1007/978-1-60761-925-3_23
Rasala B. A., Mayfield S. P. The microalga Chlamydomonas reinhardtii as a platform for the production of human protein therapeutics // Bioengineered Bugs. – 2011. – Vol. 2, iss. 1. – P. 50–54. – https://doi.org/10.4161/bbug.2.1.13423
Rathod J. P., Gade R. M., Rathod D. R., Dudhare M. A review on molecular tools of microalgal genetic transformation and their application for overexpression of different genes // International Journal of Current Microbiology and Applied Sciences. – 2017. – Vol. 6, nr 12. – P. 3191–3207. – https://doi.org/10.20546/ijcmas.2017.612.373
Ravindran B., Kurade M. B., Kabra A. N., Jeon B.-H., Gupta S. K. Recent advances and future prospects of microalgal lipid biotechnology // Algal Biofuels : Recent Advances and Future Prospects / eds: S. Gupta [et al.]. – Cham, Switzerland : Springer, 2017. – P. 1–37. – https://doi.org/10.1007/978-3-319-51010-1
Rohr J., Sarkar N., Balenger S., Jeong B. R., Cerutti H. Tandem inverted repeat system for selection of effective transgenic RNAi strains in Chlamydomonas // Plant Journal. – 2004. – Vol. 40, iss. 4. – P. 611–621. – https://doi.org/10.1111/j.1365-313X.2004.02227.x
Rosales-Mendoza S., Paz-Maldonado L. M. T., Soria-Guerra R. E. Chlamydomonas reinhardtii as a viable platform for the production of recombinant proteins: current status and perspectives // Plant Cell Reports. – 2012. – Vol. 31, iss. 3. – P. 479−494. – https://doi.org/10.1007/s00299-0111186-8
Russo M. T., Rogato A., Jaubert M., Karas B. J., Falciatore A. Phaeodactylum tricornutum: an established model species for diatom molecular research and an emerging chassis for algal synthetic biology // Journal of Phycology. – 2023. – Vol. 59, iss. 6. – P. 1114–1122. – https://doi.org/10.1111/jpy.13400
Scaife M. A., Smith A. G. Towards developing algal synthetic biology // Biochemical Society Transactions. – 2016. – Vol. 44, iss. 3. – P. 716–722. – https://doi.org/10.1042/BST20160061
Scranton M. A., Ostrand J. T., Fields F. J., Mayfield S. P. Chlamydomonas as a model for biofuels and bioproducts production // Plant Journal. – 2015. – Vol. 82, iss. 3. – P. 523–531. – https://doi.org/10.1111/tpj.12780
Shalem O., Sanjana N. E., Zhang F. High-throughput functional genomics using CRISPR-Cas9 // Nature Reviews Genetics. – 2015. – Vol. 16, iss. 5. – P. 299–311. – https://doi.org/10.1038/nrg3899
Sharma A. K., Nymark M., Sparstad T., Bones A. M., Winge P. Transgene-free genome editing in marine algae by bacterial conjugation — comparison with biolistic CRISPR/Cas9 transformation // Scientific Reports. – 2018. – Vol. 8. – Art. 14401. – https://doi.org/10.1038/s41598-018-32342-0
Sharon-Gojman R., Maimon E., Leu S., Zarka A., Boussiba S. Advanced methods for genetic engineering of Haematococcus pluvialis (Chlorophyceae, Volvocales) // Algal Research. – 2015. – Vol. 10. – P. 8–15. – https://doi.org/10.1016/j.algal.2015.03.022
Shimogawara K., Fujiwara S., Grossman A., Usuda H. High-efficiency transformation of Chlamydomonas reinhardtii by electroporation // Genetics. – 1998. – Vol. 148, iss. 4. – P. 1821–1828. – https://doi.org/10.1093/genetics/148.4.1821
Siddiqui A., Wei Z., Boehm M., Ahmad N. Engineering microalgae through chloroplast transformation to produce high‐value industrial products // Biotechnology and Applied Biochemistry. – 2020. – Vol. 67, iss. 1. – P. 30–40. – https://doi.org/10.1002/bab.1823
Simon D. P., Anila N., Gayathri K., Sarada R. Heterologous expression of β-carotene hydroxylase in Dunaliella salina by Agrobacterium-mediated genetic transformation // Algal Research. – 2016. – Vol. 18. – P. 257–265. – https://doi.org/10.1016/j.algal.2016.06.017
Sizova I., Greiner A., Awasthi M., Kateriya S., Hegemann P. Nuclear gene targeting in Chlamydomonas usingengineeredzinc‐fingernucleases//PlantJournal.–2013.–Vol.73,iss.5.– P. 873–882. – https://doi.org/10.1111/tpj.12066
Slattery S. S., Giguere D. J., Stuckless E. E., Shrestha A., Briere L.-A. K., Galbraith A., Reaume S., Boyko X., Say H. H., Browne T. S., Frederick M. I., Lant J. T., Heinemann I. U., O’Donoghue P., Dsouza L., Martin S., Howard P., Jedeszko C., Ali K., Styba J., Flatley M., Karas B. J., Gloor G. B., Edgell D. R. Phosphate-regulated expression of the SARS-CoV-2 receptor-binding domain in the diatom Phaeodactylum tricornutum for pandemic diagnostics // Scientific Reports. – 2022. – Vol. 12. – Art. 7010. – https://doi.org/10.1038/s41598-022-11053-7
Slattery S. S., Wang H., Giguere D. J., Kocsis C., Urquhart B. L., Karas B. J., Edgell D. R. Plasmid-based complementation of large deletions in Phaeodactylum tricornutum biosynthetic genes generated by Cas9 editing // Scientific Reports. – 2020. – Vol. 10. – Art. 13879. – https://doi.org/10.1038/s41598-020-70769-6
Sobieh S. S., Abed El-Gammal R., Abu El-Kheir W. S., El-Sheimy A. A., Said A. A., El-Ayouty Y. M. Heterologous expression of cyanobacterial cyanase gene (CYN) in microalga Chlamydomonas reinhardtii for bioremediation of cyanide pollution // Biology. – 2022. – Vol. 11, iss. 10. – P. 1420. – https://doi.org/10.3390/biology11101420
Solovchenko A. E. Recent breakthroughs in the biology of astaxanthin accumulation by microalgal cell // Photosynthesis Research. – 2015. – Vol. 125, iss. 3. – P. 437–449. – https://doi.org/10.1007/s11120-015-0156-3
Somchai P., Jitrakorn S., Thitamadee S., Meetam M., Saksmerprome V. Use of microalgae Chlamydomonas reinhardtii for production of double-stranded RNA against shrimp virus // Aquaculture Reports. – 2016. – Vol. 3. – P. 178–183. – https://doi.org/10.1016/j.aqrep.2016.03.003
Sonani R. R., Patel S., Bhastana B., Jakharia K., Chaubey M. G., Singh N. K., Madamwar D. Purification and antioxidant activity of phycocyanin from Synechococcus sp. R42DM isolated from industrially polluted site // Bioresource Technology. – 2017. – Vol. 245, pt. A. – P. 325–331. – https://doi.org/10.1016/j.biortech.2017.08.129
Song Y., Wang F., Chen L., Zhang W. Engineering fatty acid biosynthesis in microalgae: recent progress and perspectives // Marine Drugs. – 2024. – Vol. 22, iss. 5. – Art. 216. – https://doi.org/10.3390/md22050216
Steinbrenner J., Sandmann G. Transformation of the green alga Haematococcus pluvialis with a phytoene desaturase for accelerated astaxanthin biosynthesis // Applied and Environmental Microbiology. – 2006. – Vol. 72, iss. 12. – P. 7477–7484. – https://doi.org/10.1128/AEM.01461-06
Sun H., Wu T., Chen S. H. Y., Ren Y., Yang S., Huang J., Mou H., Chen F. Powerful tools for productivity improvements in microalgal production // Renewable and Sustainable Energy Reviews. – 2021. – Vol. 152. – Art. 111609. – https://doi.org/10.1016/j.rser.2021.111609
Sun T., Li S., Song X., Diao J., Chen L., Zhang W. Toolboxes for cyanobacteria: recent advances and future direction // Biotechnology Advances. – 2018. – Vol. 36, iss. 4. – P. 1293–1307. – https://doi.org/10.1016/j.biotechadv.2018.04.007
Tabassum B., Yousaf I., Adeyinka O. S., Khalid R., Khan A. The concept of chloroplast transformation; Its relevance towards food security // Advancements in Life Sciences. – 2024. – Vol. 11, no. 1. – P. 28–39. – URL: https://www.als-journal.com/1114-24. – Publ. date: 25.02.2024.
Talebi A. F., Tohidfar M., Bagheri A., Lyon S. R., Salehi-Ashtiani K., Tabatabaei M. Manipulation of carbon flux into fatty acid biosynthesis pathway in Dunaliella salina using AccD and ME genes to enhance lipid content and to improve produced biodiesel quality // Biofuel Research Journal. – 2014. – Vol. 1, iss. 3. – P. 91–97. – https://doi.org/10.18331/BRJ2015.1.3.6
Tissot-Lecuelle G., Purton S., Dubald M., Goldschmidt-Clermont P. Synthesisofrecombinantproducts in the chloroplast // Plastid Biology / eds: S. M. Theg, F.-A. Wollman. – New York : Springer, 2014. – P. 517–558. – https://doi.org/10.1007/978-1-4939-1136-3_18
Tran N. T., Kaldenhoff R. Achievements and challenges of genetic engineering of the model green alga Chlamydomonas reinhardtii // Algal Research. – 2020. – Vol. 50. – Art. 101986. – https://doi.org/10.1016/j.algal.2020.101986
Tran P. T., Sharifi M. N., Poddar S., Dent R. M., Niyogi K. K. Intragenic enhancers and suppressors of phytoene desaturase mutations in Chlamydomonas reinhardtii // PLOS ONE. – 2012. – Vol. 7, nr 8. – Art. e42196. – https://doi.org/10.1371/journal.pone.0042196
Trentacoste E. M., Shrestha R. P., Smith S. R., Glé C., Hartmann A. C., Hildebrand M., Gerwick W. H. Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth // Proceedings of the National Academy of Sciences of the USA. – 2013. – Vol. 110, no. 49. – P. 19748–19753. – https://doi.org/10.1073/pnas.1309299110
Verma D., Daniell H. Chloroplast vector systems for biotechnology applications // Plant Physiology. – 2007. – Vol. 145, iss. 4. – P. 1129–1143. – https://doi.org/10.1104/pp.107.106690
Virolle C., Goldlust K., Djermoun S., Bigot S., Lesterlin C. Plasmid transfer by conjugation in gramnegative bacteria: from the cellular to the community level // Genes. – 2020. – Vol. 11, iss. 11. – Art. 1239. – https://doi.org/10.3390/genes11111239
Wang B., Wang J., Zhang W., Meldrum D. R. Application of synthetic biology in cyanobacteria and algae // Frontiers in Microbiology. – 2012. – Vol. 3. – Art. 344. – https://doi.org/10.3389/fmicb.2012.00344
Wang Q., Lu Y., Xin Y., Wei L., Huang S., Xu J. Genome editing of model oleaginous microalgae Nannochloropsis spp. by CRISPR/Cas9 // Plant Journal. – 2016. – Vol. 88, iss. 6. – P. 1071–1081. – https://doi.org/10.1111/tpj.13307
Wang S., Wu S., Yang G., Pan K., Wang L., Hu Z. A review on the progress, challenges and prospects in commercializing microalgal fucoxanthin // Biotechnology Advances. – 2021. – Vol. 53. – Art. 107865. – https://doi.org/10.1016/j.biotechadv.2021.107865
Webster L. J., Villa-Gomez D., Brown R., Clarke W., Schenk P. M. A synthetic biology approach for the treatment of pollutants with microalgae // Frontiers in Bioengineering and Biotechnology. – 2024. – Vol. 12. – Art. 1379301. – https://doi.org/10.3389/fbioe.2024.1379301
Wei L., Xin Y., Wang Q., Yang J., Hu H., Xu J. RNAi-based targeted gene knockdown in the model oleaginous microalgae Nannochloropsis oceanica // Plant Journal. – 2017. – Vol. 89, iss. 6. – P. 1236–1250. – https://doi.org/10.1111/tpj.13411
Worden A. Z., Follows M. J., Giovannoni S. J., Wilken S., Zimmerman A. E., Keeling P. J. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes // Science. – 2015. – Vol. 347, № 6223. – Art. 1257594. – https://doi.org/10.1126/science.1257594
Xin Y., Wu S., Miao C., Xu T., Lu Y. Towards lipid from microalgae: products, biosynthesis, and genetic engineering // Life. – 2024. – Vol. 14, iss. 4. – Art. 447. – https://doi.org/10.3390/life14040447
Xu K., Zou W., Peng B., Guo C., Zou X. Lipid droplets from plants and microalgae: characteristics, extractions, and applications // Biology. – 2023. – Vol. 12, iss. 4. – P. 594. – https://doi.org/10.3390/biology12040594
Xu X., Gu X., Wang Zhon, Shatner W., Wang Zhen. Progress, challenges and solutions of research on photosynthetic carbon sequestration efficiency of microalgae // Renewable and Sustainable Energy Reviews. – 2019. – Vol. 110. – P. 65–82. – https://doi.org/10.1016/j.rser.2019.04.050
Xue J., Balamurugan S., Li D.-W., Liu Y.-H., Zeng H., Wang L., Yang W.-D., Liu J.-S., Li H.-Y. Glucose-6-phosphate dehydrogenase as a target for highly efficient fatty acid biosynthesis in microalgae by enhancing NADPH supply // Metabolic Engineering. – 2017. – Vol. 41. – P. 212–221. – https://doi.org/10.1016/j.ymben.2017.04.008
Yuan G., Xu X., Zhang Wei, Zhang Wenlei, Cui Y., Qin S., Liu T. Biolistic transformation of Haematococcus pluvialis with constructs based on the flanking sequences of its endogenous alpha tubulin gene // Frontiers in Microbiology. – 2019. – Vol. 10. – Art. 1749. – https://doi.org/10.3389/fmicb.2019.01749
Zabawinski C., Van Den Koornhuyse N., D’Hulst C., Schlichting R., Giersch C., Delrue B., Lacroix J. M., Preiss J., Ball S. Starchless mutants of Chlamydomonas reinhardtii lack the small subunit of a heterotetrameric ADP-glucose pyrophosphorylase // Journal of Bacteriology. – 2001. – Vol. 183, iss. 3. – P. 1069–1077. – https://doi.org/10.1128/JB.183.3.1069-1077.2001
Zhang J., Hao Q., Bai L., Xu J., Yin W., Song L., Xu L., Guo X., Fan C., Chen Y., Ruan J., Hao S., Li Y., Wang R., Hu Z. Overexpression of the soybean transcription factor GmDof4 significantly enhances the lipid content of Chlorella ellipsoidea // Biotechnology for Biofuels. – 2014. – Vol. 7, iss. 1. – Art. 128. – https://doi.org/10.1186/s13068-014-0128-4
Zhang Y., Ye Y., Bai F., Liu J. The oleaginous astaxanthin-producing alga Chromochloris zofingiensis: potential from production to an emerging model for studying lipid metabolism and carotenogenesis // Biotechnology for Biofuels. – 2021. – Vol. 14, iss. 1. – Art. 119. – https://doi.org/10.1186/s13068021-01969-z
Zulu N. N., Zienkiewicz K., Vollheyde K., Feussner I. Current trends to comprehend lipid metabolism in diatoms // Progress in Lipid Research. – 2018. – Vol. 70. – P. 1–16. – https://doi.org/10.1016/j.plipres.2018.03.001