Home > Archive>Volume 50, Issue 11, 2023 >5150-5171. DOI:10.13344/j.microbiol.china.230268
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The enhanced docosahexaenoic acid production by thraustochytrids through environmental stresses: a review
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    Abstract:

    Thraustochytrids, capable of producing multiple high-value natural active substances, such as eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), squalene, and carotenoids, have been recognized as an excellent source for commercial lipid production. Firstly, this paper briefed the ecological roles and biotechnological values of thraustochytrids and summarized two biosynthetic pathways of fatty acids. Secondly, we introduced the effects of NaCl, temperature, dissolved oxygen, and pH on the growth, lipid accumulation, fatty acid composition, and DHA production of thraustochytrids. Thirdly, we reviewed the research progress in the strategies for enhancing the DHA biosynthesis ability of thraustochytrids by osmotic regulation, staged fermentation, and alleviating oxidative stress based on environmental stress factors. Finally, we pointed out the existing problems in the current research on the molecular regulation mechanism, staged fermentation strategies, strain improvement, and metabolic engineering of thraustochytrids under environmental stresses, provided solutions for these problems, and prospected the possible development direction in the future. Overall, this review aimed to provide a practical reference for efficient industrial production of DHA by thraustochytrids.

    Reference
    [1] ROLLIN S, GUPTA A, PURI M. Optimising pineapple filtrate assisted cell disruption of wet thraustochytrid biomass for improved lipid extraction[J]. Journal of Cleaner Production, 2022, 378:134393.
    [2] WATANABE T, SAKIYAMA R, IIMI Y, SEKINE S, ABE E, NOMURA KH, NOMURA K, ISHIBASHI Y, OKINO N, HAYASHI M, ITO M. Regulation of TG accumulation and lipid droplet morphology by the novel TLDP1 in Aurantiochytrium limacinum F26-B[J]. Journal of Lipid Research, 2017, 58(12):2334-2347.
    [3] SUI N, WANG Y, LIU SS, YANG Z, WANG F, WAN SB. Transcriptomic and physiological evidence for the relationship between unsaturated fatty acid and salt stress in peanut[J]. Frontiers in Plant Science, 2018, 9:7.
    [4] CHAUHAN AS, PATEL AK, CHEN CW, CHANG JS, MICHAUD P, DONG CD, SINGHANIA RR. Enhanced production of high-value polyunsaturated fatty acids (PUFAs) from potential thraustochytrid Aurantiochytrium sp.[J]. Bioresource Technology, 2023, 370:128536.
    [5] KALIDASAN K, VINITHKUMAR NV, PETER DM, DHARANI G, DUFOSSÉ L. Thraustochytrids of mangrove habitats from Andaman Islands:species diversity, PUFA profiles and biotechnological potential[J]. Marine Drugs, 2021, 19(10):571.
    [6] BIE NN, HAN LR, MENG M, YAN ZL, WANG CL. The immunomodulatory effect of docosahexaenoic acid (DHA) on the RAW264.7 cells by modification of the membrane structure and function[J]. Food & Function, 2020, 11(3):2603-2616.
    [7] GHASEMI FARD S, WANG FL, SINCLAIR AJ, ELLIOTT G, TURCHINI GM. How does high DHA fish oil affect health? A systematic review of evidence[J]. Critical Reviews in Food Science and Nutrition, 2019, 59(11):1684-1727.
    [8] 黄淑婷, 李宏新, 于越, 袁彪, 曹崇江, 程抒劼. DHA藻油的生理功能及在食品中复配协同应用的研究进展[J]. 食品工业科技, 2023, 44(6):468-476. HUANG ST, LI HX, YU Y, YUAN B, CAO CJ, CHENG SJ. Research progress on physiological functions of DHA algal oil and its synergistic application in food[J]. Science and Technology of Food Industry, 2023, 44(6):468-476(in Chinese).
    [9] OLIVER L, DIETRICH T, MARAÑÓN I, VILLARÁN MC, BARRIO RJ. Producing omega-3 polyunsaturated fatty acids:a review of sustainable sources and future trends for the EPA and DHA market[J]. Resources, 2020, 9(12):148.
    [10] GUPTA A, BARROW CJ, PURI M. Multiproduct biorefinery from marine thraustochytrids towards a circular bioeconomy[J]. Trends in Biotechnology, 2022, 40(4):448-462.
    [11] WANG QZ, YE HK, SEN B, XIE YX, HE YD, PARK S, WANG GY. Improved production of docosahexaenoic acid in batch fermentation by newly-isolated strains of Schizochytrium sp. and Thraustochytriidae sp. through bioprocess optimization[J]. Synthetic and Systems Biotechnology, 2018, 3(2):121-129.
    [12] XIAO R, LI X, ZHENG Y. Comprehensive study of cultivation conditions and methods on lipid accumulation of a marine protist, Thraustochytrium striatum[J]. Protist, 2018, 169(4):451-465.
    [13] JIANG JY, ZHU SY, ZHANG YT, SUN XM, HU XC, HUANG H, REN LJ. Integration of lipidomic and transcriptomic profiles reveals novel genes and regulatory mechanisms of Schizochytrium sp. in response to salt stress[J]. Bioresource Technology, 2019, 294:122231.
    [14] BAGUL VP, ANNAPURE US. Isolation of fast-growing thraustochytrids and seasonal variation on the fatty acid composition of thraustochytrids from mangrove regions of Navi Mumbai, India[J]. Journal of Environmental Management, 2021, 290:112597.
    [15] BAI MH, SEN B, WANG QZ, XIE YX, HE YD, WANG GY. Molecular detection and spatiotemporal characterization of labyrinthulomycete protist diversity in the coastal waters along the Pearl River Delta[J]. Microbial Ecology, 2019, 77(2):394-405.
    [16] LYU L, WANG QZ, WANG GY. Cultivation and diversity analysis of novel marine thraustochytrids[J]. Marine Life Science & Technology, 2021, 3(2):263-275.
    [17] RAGHUKUMAR S. Ecology of the marine protists, the labyrinthulomycetes (thraustochytrids and labyrinthulids)[J]. European Journal of Protistology, 2002, 38(2):127-145.
    [18] MARCHAN LF, CHANG KJL, NICHOLS PD, MITCHELL WJ, POLGLASE JL, GUTIERREZ T. Taxonomy, ecology and biotechnological applications of thraustochytrids:a review[J]. Biotechnology Advances, 2018, 36(1):26-46.
    [19] LIU Y, SINGH P, SUN Y, LUAN SJ, WANG GY. Culturable diversity and biochemical features of thraustochytrids from coastal waters of Southern China[J]. Applied Microbiology and Biotechnology, 2014, 98(7):3241-3255.
    [20] 李晶晶, 刘瑛, 成家杨, Maurycy Daroch. 深圳海域6株破囊壶菌的生长特性及油脂成分分析[J]. 微生物学通报, 2015, 42(1):17-23. LI JJ, LIU Y, CHENG JY, MAURYCY D. Growth features and fatty acid analysis of six thraustochytrid strains from Shenzhen coastal seawater[J]. Microbiology China, 2015, 42(1):17-23(in Chinese).
    [21] SIRIRAK K, SUANJIT S, POWTONGSOOK S, JARITKHUAN S. Characterization and PUFA production of Aurantiochytrium limacinum BUCHAXM 122 isolated from fallen mangrove leaves[J]. ScienceAsia, 2020, 46(4):403-411.
    [22] JUNTILA DJ, YONEDA K, SUZUKI I. Genetic modification of the thraustochytrid Aurantiochytrium sp. 18W-13a for cellobiose utilization by secretory expression of β-glucosidase from Aspergillus aculeatus[J]. Algal Research, 2019, 40:101503.
    [23] SUN XM, XU YS, HUANG H. Thraustochytrid cell factories for producing lipid compounds[J]. Trends in Biotechnology, 2021, 39(7):648-650.
    [24] SOUDANT P, VENTURA M, CHAUCHAT L, GUERREIRO M, MATHIEU-RESUGE M, Le GRAND F, SIMON V, COLLET S, ZAMBONINO-INFANTE JL, Le GOÏC N, LAMBERT C, FERNANDES F, SILKINA A, de SOUZA MF, de la BROISE D. Evaluation of Aurantiochytrium mangrovei biomass grown on digestate as a sustainable feed ingredient of sea bass, Dicentrarchus labrax, juveniles and larvae[J]. Sustainability, 2022, 14(21):14573.
    [25] LI J, LIU RJ, CHANG GF, LI XY, CHANG M, LIU YF, JIN QZ, WANG XG. A strategy for the highly efficient production of docosahexaenoic acid by Aurantiochytrium limacinum SR21 using glucose and glycerol as the mixed carbon sources[J]. Bioresource Technology, 2015, 177:51-57.
    [26] GUO DS, JI XJ, REN LJ, LI GL, HUANG H. Improving docosahexaenoic acid production by Schizochytrium sp. using a newly designed high-oxygen-supply bioreactor[J]. AIChE Journal, 2017, 63(10):4278-4286.
    [27] JU JH, OH BR, KO DJ, HEO SY, LEE JJ, KIM YM, YANG K, SEO JW, HONG WK, KIM CH. Boosting productivity of heterotrophic microalgae by efficient control of the oxygen transfer coefficient using a microbubble sparger[J]. Algal Research, 2019, 41:101474.
    [28] QU L, REN LJ, HUNG H. Scale-up of docosahexaenoic acid production in fed-batch fermentation by Schizochytrium sp. based on volumetric oxygen-transfer coefficient[J]. Biochemical Engineering Journal, 2013, 77:82-87.
    [29] GUO DS, JI XJ, REN LJ, LI GL, SUN XM, CHEN KQ, GAO S, HUANG H. Development of a scale-up strategy for fermentative production of docosahexaenoic acid by Schizochytrium sp.[J]. Chemical Engineering Science, 2018, 176:600-608.
    [30] CHANG GF, GAO NS, TIAN GW, WU QH, CHANG M, WANG XG. Improvement of docosahexaenoic acid production on glycerol by Schizochytrium sp. S31 with constantly high oxygen transfer coefficient[J]. Bioresource Technology, 2013, 142:400-406.
    [31] GUO DS, TONG LL, JI XJ, REN LJ, DING QQ. Development of a strategy to improve the stability of culture environment for docosahexaenoic acid fermentation by Schizochytrium sp.[J]. Applied Biochemistry and Biotechnology, 2020, 192(3):881-894.
    [32] XU XD, HUANG CY, XU ZX, XU HX, WANG Z, YU XJ. The strategies to reduce cost and improve productivity in DHA production by Aurantiochytrium sp.:from biochemical to genetic respects[J]. Applied Microbiology and Biotechnology, 2020, 104(22):9433-9447.
    [33] CHEN XH, SEN B, ZHANG S, BAI MH, HE YD, WANG GY. Chemical and physical culture conditions significantly influence the cell mass and docosahexaenoic acid content of Aurantiochytrium limacinum strain PKU#SW8[J]. Marine Drugs, 2021, 19(12):671.
    [34] QU L, REN LJ, SUN GN, JI XJ, NIE ZK, HUANG H. Batch, fed-batch and repeated fed-batch fermentation processes of the marine thraustochytrid Schizochytrium sp. for producing docosahexaenoic acid[J]. Bioprocess and Biosystems Engineering, 2013, 36(12):1905-1912.
    [35] WANG S, WAN WJ, WANG ZJ, ZHANG HD, LIU H, ARUNAKUMARA KKIU, CUI Q, SONG XJ. A two-stage adaptive laboratory evolution strategy to enhance docosahexaenoic acid synthesis in oleaginous thraustochytrid[J]. Frontiers in Nutrition, 2021, 8:795491.
    [36] HAN X, LI ZH, WEN Y, CHEN Z. Overproduction of docosahexaenoic acid in Schizochytrium sp. through genetic engineering of oxidative stress defense pathways[J]. Biotechnology for Biofuels, 2021, 14(1):70.
    [37] SHUIB S, NAZIR MYM, IBRAHIM I, SONG YD, RATLEDGE C, HAMID AA. Co-existence of type I fatty acid synthase and polyketide synthase metabolons in Aurantiochytrium SW1 and their implications for lipid biosynthesis[J]. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 2022, 1867(12):159224.
    [38] HEGGESET TMB, ERTESVÅG H, LIU B, ELLINGSEN TE, VADSTEIN O, AASEN IM. Lipid and DHA-production in Aurantiochytrium sp.- responses to nitrogen starvation and oxygen limitation revealed by analyses of production kinetics and global transcriptomes[J]. Scientific Reports, 2019, 9:19470.
    [39] MORABITO C, BOURNAUD C, MAËS C, SCHULER M, AIESE CIGLIANO R, DELLERO Y, MARÉCHAL E, AMATO A, RÉBEILLÉ F. The lipid metabolism in thraustochytrids[J]. Progress in Lipid Research, 2019, 76:101007.
    [40] RATLEDGE C. Fatty acid biosynthesis in microorganisms being used for single cell oil production[J]. Biochimie, 2004, 86(11):807-815.
    [41] WANG FZ, BI YL, DIAO JJ, LÜ MM, CUI JY, CHEN L, ZHANG WW. Metabolic engineering to enhance biosynthesis of both docosahexaenoic acid and odd-chain fatty acids in Schizochytrium sp. S31[J]. Biotechnology for Biofuels, 2019, 12:141.
    [42] LIANG YM, LIU Y, TANG J, MA J, CHENG JJ, DAROCH M. Transcriptomic profiling and gene disruption revealed that two genes related to PUFAs/DHA biosynthesis may be essential for cell growth of Aurantiochytrium sp.[J]. Marine Drugs, 2018, 16(9):310.
    [43] PRABHAKARAN P, RAETHONG N, NAZIR Y, HALIM H, YANG W, VONGSANGNAK W, HAMID AA, SONG YD. Whole genome analysis and elucidation of docosahexaenoic acid (DHA) biosynthetic pathway in Aurantiochytrium sp. SW1[J]. Gene, 2022, 846:146850.
    [44] LIPPMEIER JC, CRAWFORD KS, OWEN CB, RIVAS AA, METZ JG, APT KE. Characterization of both polyunsaturated fatty acid biosynthetic pathways in Schizochytrium sp.[J]. Lipids, 2009, 44(7):621-630.
    [45] HU F, CLEVENGER AL, ZHENG P, HUANG QY, WANG ZK. Low-temperature effects on docosahexaenoic acid biosynthesis in Schizochytrium sp. TIO01 and its proposed underlying mechanism[J]. Biotechnology for Biofuels, 2020, 13(1):172.
    [46] DU F, WANG YZ, XU YS, SHI TQ, LIU WZ, SUN XM, HUANG H. Biotechnological production of lipid and terpenoid from thraustochytrids[J]. Biotechnology Advances, 2021, 48:107725.
    [47] SHABALA L, McMEEKIN T, SHABALA S. Osmotic adjustment and requirement for sodium in marine protist thraustochytrid[J]. Environmental Microbiology, 2009, 11(7):1835-1843.
    [48] CHEN CY, LEE MH, DONG CD, LEONG YK, CHANG JS. Enhanced production of microalgal lipids using a heterotrophic marine microalga Thraustochytrium sp. BM2[J]. Biochemical Engineering Journal, 2020, 154:107429.
    [49] YOKOCHI T, HONDA D, HIGASHIHARA T, NAKAHARA T. Optimization of docosahexaenoic acid production by Schizochytrium limacinum SR21[J]. Applied Microbiology and Biotechnology, 1998, 49(1):72-76.
    [50] CHEN W, ZHOU PP, ZHU YM, XIE C, MA L, WANG XP, BAO ZD, YU LJ. Improvement in the docosahexaenoic acid production of Schizochytrium sp. S056 by replacement of sea salt[J]. Bioprocess and Biosystems Engineering, 2016, 39(2):315-321.
    [51] UNAGUL P, ASSANTACHAI C, PHADUNGRUENGLUIJ S, PONGSUTEERAGUL T, SUPHANTHARIKA M, VERDUYN C. Biomass and docosahexaenoic acid formation by Schizochytrium mangrovei Sk-02 at low salt concentrations[J]. Botanica Marina, 2006, 49(2):182-190.
    [52] SUN XM, REN LJ, BI ZQ, JI XJ, ZHAO QY, HUANG H. Adaptive evolution of microalgae Schizochytrium sp. under high salinity stress to alleviate oxidative damage and improve lipid biosynthesis[J]. Bioresource Technology, 2018, 267:438-444.
    [53] UNAGUL P, ASSANTACHAI C, PHADUNGRUENGLUIJ S, SUPHANTHARIKA M, VERDUYN C. Properties of the docosahexaenoic acid-producer Schizochytrium mangrovei Sk-02:effects of glucose, temperature and salinity and their interaction[J]. Botanica Marina, 2005, 48(5/6):387-394.
    [54] HUANG JJH, CHEUNG PCK. Cold stress treatment enhances production of metabolites and biodiesel feedstock in Porphyridium cruentum via adjustment of cell membrane fluidity[J]. Science of the Total Environment, 2021, 780:146612.
    [55] CUNHA E, SOUSA V, GEADA P, TEIXEIRA JA, VICENTE AA, DIAS O. Systems biology's role in leveraging microalgal biomass potential:current status and future perspectives[J]. Algal Research, 2023, 69:102963.
    [56] 刘静, 高媛媛, 江贤章, 毛若雨, 田宝玉, 柯崇榕, 吴松刚, 黄建忠. 低温胁迫对裂殖壶菌DHA生物合成及SOD表达的影响[J]. 药物生物技术, 2010, 17(1):50-55. LIU J, GAO YY, JIANG XZ, MAO RY, TIAN BY, KE CR, WU SG, HUANG JZ. Effects on docosahexaenoic acid biosynthesis and expression of superoxide dismutase in Schizochytrium at low temperature[J]. Pharmaceutical Biotechnology, 2010, 17(1):50-55(in Chinese).
    [57] ZENG Y, JI XJ, LIAN M, REN LJ, JIN LJ, OUYANG PK, HUANG H. Development of a temperature shift strategy for efficient docosahexaenoic acid production by a marine fungoid protist, Schizochytrium sp. HX-308[J]. Applied Biochemistry and Biotechnology, 2011, 164(3):249-255.
    [58] 张明亮, 王俊, 翁可欣, 李力, 黄建忠, 林清强. 变温调控破囊壶菌发酵生产二十二碳六烯酸[J]. 食品与发酵工业, 2022, 48(3):15-19. ZHANG ML, WANG J, WENG KX, LI L, HUANG JZ, LIN QQ. Docosahexaenoic acid production by Aurantiochytrium sp. FN21 under temperature shifting management[J]. Food and Fermentation Industries, 2022, 48(3):15-19(in Chinese).
    [59] YALI MP, JALILI H, NOROOZI M, MORADI Y, SABA F. Optimization of culture conditions for growth of the Aurantiochytrium sp. shy, isolated from the Persian Gulf[J]. Iranian Journal of Fisheries Sciences, 2019, 18(4):656-671.
    [60] ZHOU PP, LU MB, LI W, YU LJ. Microbial production of docosahexaenoic acid by a low temperature-adaptive strain Thraustochytriidae sp. Z105:screening and optimization[J]. Journal of Basic Microbiology, 2010, 50(4):380-387.
    [61] 周芬, 张明亮, 黄建忠, 江贤章. 变温对破囊壶菌FJN-10脂肪酸组分和蛋白质组的影响[J]. 生物技术, 2015, 25(4):384-390. ZHOU F, ZHANG ML, HUANG JZ, JIANG XZ. Effect of temperature shift on polyunsaturated fatty acids production and proteome of Thraustochytrium sp. FJN-10[J]. Biotechnology, 2015, 25(4):384-390(in Chinese).
    [62] 任良栋, 许团辉, 徐权汉, 刘思喜, 夏伟, 张浩. 一株高产DHA菌株的筛选及其发酵条件优化[J]. 中国油脂, 2016, 41(5):60-64. REN LD, XU TH, XU QH, LIU SX, XIA W, ZHANG H. Screening and optimization of fermentation conditions of Schizochytrium strain with high-productive DHA[J]. China Oils and Fats, 2016, 41(5):60-64(in Chinese).
    [63] LIU Y, TANG J, LI JJ, DAROCH M, CHENG JJ. Efficient production of triacylglycerols rich in docosahexaenoic acid (DHA) by osmo-heterotrophic marine protists[J]. Applied Microbiology and Biotechnology, 2014, 98(23):9643-9652.
    [64] ZHANG AQ, HE YD, SEN B, WANG WJ, WANG X, WANG GY. Optimal NaCl medium enhances squalene accumulation in Thraustochytrium sp. ATCC 26185 and influences the expression levels of key metabolic genes[J]. Frontiers in Microbiology, 2022, 13:900252.
    [65] LI L, TANG XY, LUO YY, HU XC, REN LJ. Accumulation and conversion of β-carotene and astaxanthin induced by abiotic stresses in Schizochytrium sp.[J]. Bioprocess and Biosystems Engineering, 2022, 45(5):911-920.
    [66] ZHU LY, ZHANG XC, JI L, SONG XJ, KUANG CH. Changes of lipid content and fatty acid composition of Schizochytrium limacinum in response to different temperatures and salinities[J]. Process Biochemistry, 2007, 42(2):210-214.
    [67] TAOKA Y, NAGANO N, OKITA Y, IZUMIDA H, SUGIMOTO S, HAYASHI M. Influences of culture temperature on the growth, lipid content and fatty acid composition of Aurantiochytrium sp. strain mh0186[J]. Marine Biotechnology, 2009, 11(3):368-374.
    [68] PAREDES P, LARAMA G, FLORES L, LEYTON A, ILI CG, ASENJO JA, CHISTI Y, SHENE C. Temperature differentially affects gene expression in Antarctic thraustochytrid Oblongichytrium sp. RT2316-13[J]. Marine Drugs, 2020, 18(11):563.
    [69] SHENE C, PAREDES P, FLORES L, LEYTON A, ASENJO JA, CHISTI Y. Dynamic flux balance analysis of biomass and lipid production by Antarctic thraustochytrid Oblongichytrium sp. RT2316-13[J]. Biotechnology and Bioengineering, 2020, 117(10):3006-3017.
    [70] MA ZX, TAN YZ, CUI GZ, FENG YG, CUI Q, SONG XJ. Transcriptome and gene expression analysis of DHA producer Aurantiochytrium under low temperature conditions[J]. Scientific Reports, 2015, 5:14446.
    [71] 叶会科. 破囊壶菌Thraustochytriidae sp. PKU#Mn16高产DHA的发酵技术研究[D]. 天津:天津大学博士学位论文, 2020. YE HK. Thriving for higher yield of DHA through fermentation technology in Thraustochytriidae sp. PKU#Mn16[D]. Tianjin:Doctoral Dissertation of Tianjin University, 2020(in Chinese).
    [72] BI ZQ, REN LJ, HU XC, SUN XM, ZHU SY, JI XJ, HUANG H. Transcriptome and gene expression analysis of docosahexaenoic acid producer Schizochytrium sp. under different oxygen supply conditions[J]. Biotechnology for Biofuels, 2018, 11:249.
    [73] CHANG GF, WU J, JIANG CH, TIAN GW, WU QH, CHANG M, WANG XG. The relationship of oxygen uptake rate and kLa with rheological properties in high cell density cultivation of docosahexaenoic acid by Schizochytrium sp. S31[J]. Bioresource Technology, 2014, 152:234-240.
    [74] GUO DS, JI XJ, REN LJ, LI GL, YIN FW, HUANG H. Development of a real-time bioprocess monitoring method for docosahexaenoic acid production by Schizochytrium sp.[J]. Bioresource Technology, 2016, 216:422-427.
    [75] QU L, JI XJ, REN LJ, NIE ZK, FENG Y, WU WJ, OUYANG PK, HUANG H. Enhancement of docosahexaenoic acid production by Schizochytrium sp. using a two-stage oxygen supply control strategy based on oxygen transfer coefficient[J]. Letters in Applied Microbiology, 2011, 52(1):22-27.
    [76] CIPAK A, HASSLACHER M, TEHLIVETS O, COLLINSON EJ, ZIVKOVIC M, MATIJEVIC T, WONISCH W, WAEG G, DAWES IW, ZARKOVIC N, KOHLWEIN SD. Saccharomyces cerevisiae strain expressing a plant fatty acid desaturase produces polyunsaturated fatty acids and is susceptible to oxidative stress induced by lipid peroxidation[J]. Free Radical Biology and Medicine, 2006, 40(5):897-906.
    [77] CHI ZY, LIU Y, FREAR C, CHEN SL. Study of a two-stage growth of DHA-producing marine algae Schizochytrium limacinum SR21 with shifting dissolved oxygen level[J]. Applied Microbiology and Biotechnology, 2009, 81(6):1141-1148.
    [78] LIU L, ZHU XY, YE HK, WEN YY, SEN B, WANG GY. Low dissolved oxygen supply functions as a global regulator of the growth and metabolism of Aurantiochytrium sp. PKU#Mn16 in the early stages of docosahexaenoic acid fermentation[J]. Microbial Cell Factories, 2023, 22(1):52.
    [79] JAKOBSEN AN, AASEN IM, JOSEFSEN KD, STRØM AR. Accumulation of docosahexaenoic acid-rich lipid in thraustochytrid Aurantiochytrium sp. strain T66:effects of N and P starvation and O2 limitation[J]. Applied Microbiology and Biotechnology, 2008, 80(2):297-306.
    [80] AASEN IM, ERTESVÅG H, HEGGESET TMB, LIU B, BRAUTASET T, VADSTEIN O, ELLINGSEN TE. Thraustochytrids as production organisms for docosahexaenoic acid (DHA), squalene, and carotenoids[J]. Applied Microbiology and Biotechnology, 2016, 100(10):4309-4321.
    [81] MIEDEMA H, STAAL M, PRINS HA. pH-induced proton permeability changes of plasma membrane vesicles[J]. The Journal of Membrane Biology, 1996, 152(2):159-167.
    [82] AABO T, GLÜCKSTAD J, SIEGUMFELDT H, ARNEBORG N. Intracellular pH distribution as a cell health indicator in Saccharomyces cerevisiae[J]. Journal of the Royal Society, Interface, 2011, 8(64):1635-1643.
    [83] WU ST, YU ST, LIN LP. Effect of culture conditions on docosahexaenoic acid production by Schizochytrium sp. S31[J]. Process Biochemistry, 2005, 40(9):3103-3108.
    [84] ZHAO XY, REN LJ, GUO DS, WU WJ, JI XJ, HUANG H. CFD investigation of Schizochytrium sp. impeller configurations on cell growth and docosahexaenoic acid synthesis[J]. Bioprocess and Biosystems Engineering, 2016, 39(8):1297-1304.
    [85] ZHAO B, LI YF, MBIFILE MD, LI CL, YANG HL, WANG W. Improvement of docosahexaenoic acid fermentation from Schizochytrium sp. AB-610 by staged pH control based on cell morphological changes[J]. Engineering in Life Sciences, 2017, 17(9):981-988.
    [86] SHAFIQ M, ZEB L, CUI GN, JAWAD M, CHI ZY. High-density pH-auxostat fed-batch culture of Schizochytrium limacinum SR21 with acetic acid as a carbon source[J]. Applied Biochemistry and Biotechnology, 2020, 192(4):1163-1175.
    [87] YIN FW, ZHANG YT, JIANG JY, GUO DS, GAO S, GAO Z. Efficient docosahexaenoic acid production by Schizochytrium sp. via a two-phase pH control strategy using ammonia and citric acid as pH regulators[J]. Process Biochemistry, 2019, 77:1-7.
    [88] BOURAS S, ANTONIADIS D, KOUNTRIAS G, KARAPANAGIOTIDIS IT, KATSOULAS N. Effect of pH on Schizochytrium limacinum production grown using crude glycerol and biogas digestate effluent[J]. Agronomy, 2022, 12(2):364.
    [89] KHUMRANGSEE K, CHAROENRAT T, PRAIBOON J, CHITTAPUN S. Development of a fed-batch fermentation with stepwise aeration to enhance docosahexaenoic acid and carotenoid content in Aurantiochytrium sp. FIKU018[J]. Journal of Applied Phycology, 2022, 34(3):1243-1253.
    [90] KAYA K, KAZAMA Y, ABE T, SHIRAISHI F. Influence of medium components and pH on the production of odd-carbon fatty acids by Aurantiochytrium sp. SA-96[J]. Journal of Applied Phycology, 2020, 32(3):1597-1606.
    [91] WANG SK, WANG X, TIAN YT, CUI YH. Nutrient recovery from tofu whey wastewater for the economical production of docosahexaenoic acid by Schizochytrium sp. S31[J]. Science of the Total Environment, 2020, 710:136448.
    [92] YIN Y, DING Y, FENG G, LI J, XIAO L, KARUPPIAH V, SUN W, ZHANG F, LI Z. Modification of artificial sea water for the mass production of (+)-terrein by Aspergillus terreus strain PF26 derived from marine sponge Phakellia fusca[J]. Letters in Applied Microbiology, 2015, 61(6):580-587.
    [93] ZHANG AQ, MERNITZ K, WU C, XIONG W, HE YD, WANG GY, WANG X. ATP drives efficient terpene biosynthesis in marine thraustochytrids[J]. mBio, 2021, 12(3):e00881-21.
    [94] ZHANG AQ, XIE YX, HE YD, WANG WJ, SEN B, WANG GY. Bio-based squalene production by Aurantiochytrium sp. through optimization of culture conditions, and elucidation of the putative biosynthetic pathway genes[J]. Bioresource Technology, 2019, 287:121415.
    [95] SHABALA L, McMEEKIN T, SHABALA S. Thraustochytrids can be grown in low-salt media without affecting PUFA production[J]. Marine Biotechnology, 2013, 15(4):437-444.
    [96] 王澍, 吕小义, 张静雯, 田华, 陈涛, 何东平. 不同碳氮源浓度和培养温度对裂殖壶菌产DHA的影响[J]. 中国油脂, 2015, 40(10):74-77. WANG S, LYU XY, ZHANG JW, TIAN H, CHEN T, HE DP. Impacts of different concentrations of carbon and nitrogen sources and culture temperature on DHA production by Schizochytrium sp.[J]. China Oils and Fats, 2015, 40(10):74-77(in Chinese).
    [97] 王杰鹏, 罗瑶, 郗大兴. 搅拌和通气对裂殖壶菌LX0809产DHA的影响[J]. 生物加工过程, 2017, 15(1):16-19. WANG JP, LUO Y, XI DX. Effects of agitation and aeration on DHA production by Schizochytrium LX0809[J]. Chinese Journal of Bioprocess Engineering, 2017, 15(1):16-19(in Chinese).
    [98] REN LJ, JI XJ, HUANG H, QU L, FENG Y, TONG QQ, OUYANG PK. Development of a stepwise aeration control strategy for efficient docosahexaenoic acid production by Schizochytrium sp.[J]. Applied Microbiology and Biotechnology, 2010, 87(5):1649-1656.
    [99] ZHANG ML, WU WB, GUO XL, YOU WC, QI F, JIANG XZ, HUANG JZ. Mathematical modeling of fed-batch fermentation of Schizochytrium sp. FJU-512 growth and DHA production using a shift control strategy[J]. 3 Biotech, 2018, 8:162.
    [100] CHI GX, XU YY, CAO XY, LI ZP, CAO MF, CHISTI Y, HE N. Production of polyunsaturated fatty acids by Schizochytrium (Aurantiochytrium) spp.[J]. Biotechnology Advances, 2022, 55:107897.
    [101] SUN XM, REN LJ, BI ZQ, JI XJ, ZHAO QY, JIANG L, HUANG H. Development of a cooperative two-factor adaptive-evolution method to enhance lipid production and prevent lipid peroxidation in Schizochytrium sp.[J]. Biotechnology for Biofuels, 2018, 11:65.
    [102] SUN XM, GENG LJ, REN LJ, JI XJ, HAO N, CHEN KQ, HUANG H. Influence of oxygen on the biosynthesis of polyunsaturated fatty acids in microalgae[J]. Bioresource Technology, 2018, 250:868-876.
    [103] ARORA N, YEN HW, PHILIPPIDIS GP. Harnessing the power of mutagenesis and adaptive laboratory evolution for high lipid production by oleaginous microalgae and yeasts[J]. Sustainability, 2020, 12(12):5125.
    [104] MAVROMMATI M, DASKALAKI A, PAPANIKOLAOU S, AGGELIS G. Adaptive laboratory evolution principles and applications in industrial biotechnology[J]. Biotechnology Advances, 2022, 54:107795.
    [105] HU XC, TANG XY, BI ZQ, ZHAO QY, REN LJ. Adaptive evolution of microalgae Schizochytrium sp. under high temperature for efficient production of docosahexaeonic acid[J]. Algal Research, 2021, 54:102212.
    [106] SUN XM, REN LJ, JI XJ, CHEN SL, GUO DS, HUANG H. Adaptive evolution of Schizochytrium sp. by continuous high oxygen stimulations to enhance docosahexaenoic acid synthesis[J]. Bioresource Technology, 2016, 211:374-381.
    [107] REN LJ, SUN XM, JI XJ, CHEN SL, GUO DS, HUANG H. Enhancement of docosahexaenoic acid synthesis by manipulation of antioxidant capacity and prevention of oxidative damage in Schizochytrium sp.[J]. Bioresource Technology, 2017, 223:141-148.
    [108] BAO ZD, ZHU YM, FENG YM, ZHANG K, ZHANG M, WANG ZK, YU LJ. Enhancement of lipid accumulation and docosahexaenoic acid synthesis in Schizochytrium sp. H016 by exogenous supplementation of sesamol[J]. Bioresource Technology, 2022, 345:126527.
    [109] SINGH D, MATHUR AS, TULI DK, PURI M, BARROW CJ. Propyl gallate and butylated hydroxytoluene influence the accumulation of saturated fatty acids, omega-3 fatty acid and carotenoids in thraustochytrids[J]. Journal of Functional Foods, 2015, 15:186-192.
    [110] GAFFNEY M, O՚ROURKE R, MURPHY R. Manipulation of fatty acid and antioxidant profiles of the microalgae Schizochytrium sp. through flaxseed oil supplementation[J]. Algal Research, 2014, 6:195-200.
    [111] YU XJ, SUN J, SUN YQ, ZHENG JY, WANG Z. Metabolomics analysis of phytohormone gibberellin improving lipid and DHA accumulation in Aurantiochytrium sp.[J]. Biochemical Engineering Journal, 2016, 112:258-268.
    [112] ZHANG S, HE YD, SEN B, CHEN XH, XIE YX, KEASLING JD, WANG GY. Alleviation of reactive oxygen species enhances PUFA accumulation in Schizochytrium sp. through regulating genes involved in lipid metabolism[J]. Metabolic Engineering Communications, 2018, 6:39-48.
    [113] POLBRAT T, KONKOL D, KORCZYNSKI M. Optimization of docosahexaenoic acid production by Schizochytrium sp.:a review[J]. Biocatalysis and Agricultural Biotechnology, 2021, 35:102076.
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WANG Yangyang, LI Jiaqian, ZHU Xingyu, LIU Lu, WANG Guangyi. The enhanced docosahexaenoic acid production by thraustochytrids through environmental stresses: a review[J]. Microbiology China, 2023, 50(11): 5150-5171

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  • Received:April 05,2023
  • Adopted:June 14,2023
  • Online: November 06,2023
  • Published: November 20,2023
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