

FOLLOWUS
1.Tianjin Agricultural University, College of Fisheries, Tianjin Key Lab for Aquaculture Ecology and Cultivation, Tianjin 300384, China
2.Tianjin Modern Tianjiao Agricultural Technology Co., Ltd., Tianjin Key Laboratory for Green and Ecological Forage, Tianjin 301800, China
saz0908@126.com
Received:03 March 2022,
Accepted:18 April 2022,
Online First:17 June 2022,
Published:01 September 2023
Scan QR Code
DOU Yong,LI Jiayi,ZHOU Wenli.Metabolomics of astaxanthin hyperaccumulation in Haematococcuspluvialis under high light stress[J].Journal of Oceanology and Limnology,2023,41(05):1876-1886.
Variation in metabolite profiles of
Haematococcus
pluvialis
(a type of unicellular green algal) under light stress is a key issue of study at the present. To investigate the effect of light intensity on accumulation of astaxa
nthin in
H
.
pluvialis
a 26-day batch culture experiment of
H
.
pluvialis
under the light intensity levels at 73
127
182
236
and 291 μmol/(m
2
·s) was conducted. Therefore
the optimal light intensity and the corresponding metabolic pathways of accumulation in
H
.
pluvialis
were determined. Results show that 236 μmol/(m
2
·s) was the optimum light intensity to induce astaxanthin accumulation
at which a maximum content of 9.01 mg/L was achieved on Day 24. A total of 132 metabolites were identified and quantified
of which 38 differential metabolites were highlighted and classified
including 3 fatty acids or intermediates
5 amino acids or derivatives
5 carbohydrates or intermediates
16 nucleoside derivatives
and 9 other metabolites using LC-MS/MS technique. Subsequently
16 statistically significant differential metabolic pathways were enriched and annotated based on Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis between the control and the 236 μmol/(m
2
·s) treatment group (
P
<
0.05). In addition
the bioprocesses included cellular basal metabolism and signaling systems
such as carbohydrate metabolism
amino acid metabolism
glycerol and derivatives metabolism
nucleotide and derivative metabolism
and inositol phosphate metabolism were activated and regulated under strong light stress conditions. Moreover
4 hub metabolites containing D-glucose-6-phosphate
L-tyrosine
glycerol-3-phosphate
and L-glutamine were identified
based on which the associated metabolic network was constructed. The study provided a metabolomic view of astaxanthin accumulation in
H
.
pluvialis
under strong light stress.
Ak B , Işık O , Uslu L et al . 2015 . The effect of stress due to nitrogen limitation on lipid content of Phaeodactylum Tricornutum (Bohlin) cultured outdoor in photobioreactor . Turkish Journal of Fisheries and Aquatic Sciences , 15 ( 3 ): 647 - 652 , https://doi.org/10.4194/1303-2712-v15_3_09 https://doi.org/10.4194/1303-2712-v15_3_09 .
Alipanah L , Rohloff J , Winge P et al . 2015 . Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum . Journal of Experimental Botany , 66 ( 20 ): 6281 - 6296 , https://doi.org/10.1093/jxb/erv340 https://doi.org/10.1093/jxb/erv340 .
Boussiba S , Fan L , Vonshak A . 1992 . Enhancement and determination of astaxanthin accumulation in green-alge Haematococcus pluvialis . Methods in Enzymology , 213 : 386 - 391 , https://10.1016/0076-6879(92)13140-S https://10.1016/0076-6879(92)13140-S . https://do 10.1016/0076-6879(92)13140-s http://dx.doi.org/10.1016/0076-6879(92)13140-s
Cappello T . 2020 . NMR-based metabolomics of aquatic organisms . eMagRes , 9 ( 1 ): 81 - 100 , https://doi.org/10.1002/9780470034590.emrstm1604 https://doi.org/10.1002/9780470034590.emrstm1604 .
Chen G Q , Wang B B , Han D X et al . 2015 . Molecular mechanisms of the coordination between astaxanthin and fatty acid biosynthesis in Haematococcus pluvialis (Chlorophyceae) . The Plant Journal , 81 ( 1 ): 95 - 107 , https://doi.org/10.1111/tpj.12713 https://doi.org/10.1111/tpj.12713 .
Chen Z , Chen J , Liu J H et al . 2020 . Transcriptomic and metabolic analysis of an astaxanthin-hyperproducing Haematococcus pluvialis mutant obtained by low-temperature plasma (LTP) mutagenesis under high light irradiation . Algal Research , 45 : 101746 , https://doi.org/10.1016/j.algal.2019.101746 https://doi.org/10.1016/j.algal.2019.101746 .
Christian D , Zhang J , Sawdon A J et al . 2018 . Enhanced astaxanthin accumulation in Haematococcus pluvialis using high carbon dioxide concentration and light illumination . Bioresource Technology , 256 : 548 - 551 , https://doi.org/10.1016/j.biortech.2018.02.074 https://doi.org/10.1016/j.biortech.2018.02.074 .
Ding W , Cui J , Zhao Y T et al . 2019a . Enhancing Haematococcus pluvialis biomass and γ-aminobutyric acid accumulation by two-step cultivation and salt supplementation . Bioresource Technology , 285 : 121334 , https://doi.org/10.1016/j.biortech.2019.121334 https://doi.org/10.1016/j.biortech.2019.121334 .
Ding W , Li Q Q , Han B Y et al . 2019b . Comparative physiological and metabolomic analyses of the hyper-accumulation of astaxanthin and lipids in Haematococcus pluvialis upon treatment with butylatedhydroxyanisole . Bioresource Technology , 292 : 122002 , https://doi.org/10.1016/j.biortech.2019.122002 https://doi.org/10.1016/j.biortech.2019.122002 .
Ding W , Zhao P , Peng J et al . 2018 . Melatonin enhances astaxanthin accumulation in the green microalga Haematococcus pluvialis by mechanisms possibly related to abiotic stress tolerance . Algal Research , 33 : 256 - 265 , https://doi.org/10.1016/j.algal.2018.05.021 https://doi.org/10.1016/j.algal.2018.05.021 .
Dunn W B , Ellis D I . 2005 . Metabolomics: current analytical platforms and methodologies . TrAC Trends in Analytical Chemistry , 24 ( 4 ): 285 - 294 , https://doi.org/10.1016/j.trac.2004.11.021 https://doi.org/10.1016/j.trac.2004.11.021 . https://do 10.1016/j.trac.2004.11.021 http://dx.doi.org/10.1016/j.trac.2004.11.021
Fang N , Wang C K , Liu X F et al . 2019 . De novo synthesis of astaxanthin: from organisms to genes . Trends in Food Science & Technology , 92 : 162 - 171 , https://doi.org/10.1016/j.tifs.2019.08.016 https://doi.org/10.1016/j.tifs.2019.08.016 .
Fernandes B , Teixeira J , Dragone G et al . 2013 . Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri . Bioresource Technology , 144 : 268 - 274 , https://doi.org/10.1016/j.biortech.2013.06.096 https://doi.org/10.1016/j.biortech.2013.06.096 .
Goiris K , Muylaert K , Fraeye I et al . 2012 . Antioxidant potential of microalgae in relation to their phenolic and carotenoid content . Journal of Applied Phycology , 24 ( 6 ): 1477 - 1486 , https://doi.org/10.1007/s10811-012-9804-6 https://doi.org/10.1007/s10811-012-9804-6 .
Goyal A . 2007 . Osmoregulation in Dunaliella , Part II: photosynthesis and starch contribute carbon for glycerol synthesis during a salt stress in Dunaliella tertiolecta . Plant Physiology and Biochemistry , 45 ( 9 ): 705 - 710 , https://doi.org/10.1016/j.plaphy.2007.05.009 https://doi.org/10.1016/j.plaphy.2007.05.009 .
Hollywood K , Brison D R , Goodacre R . 2006 . Metabolomics: current technologies and future trends . Proteomics , 6 ( 17 ): 4716 - 4723 , https://doi.org/10.1002/pmic.200600106 https://doi.org/10.1002/pmic.200600106 .
Holtin K , Kuehnle M , Rehbein J et al . 2009 . Determination of astaxanthin and astaxanthin esters in the microalgae Haematococcus pluvialis by LC-(APCI) MS and characterization of predominant carotenoid isomers by NMR spectroscopy . Analytical and Bioanalytical Chemistry , 395 ( 6 ): 1613 - 1622 , https://doi.org/10.1007/s00216-009-2837-2 https://doi.org/10.1007/s00216-009-2837-2 .
Kanehisa M , Araki M , Goto S et al . 2008 . KEGG for linking genomes to life and the environment . Nucleic Acids Research , 36 : D480 - D484 , https://doi.org/10.1093/nar/gkm882 https://doi.org/10.1093/nar/gkm882 .
Kobayashi M , Sakamoto Y . 1999 . Singlet oxygen quenching ability of astaxanthin esters from the green alga Haematococcus pluvialis . Biotechnology Letters , 21 ( 4 ): 265 - 269 , https://doi.org/10.1023/A:1005445927433 https://doi.org/10.1023/A:1005445927433 .
Kokabi K , Gorelova O , Ismagulova T et al . 2019 . Metabolomic foundation for differential responses of lipid metabolism to nitrogen and phosphorus deprivation in an arachidonic acid-producing green microalga . Plant Science , 283 : 95 - 115 , https://doi.org/10.1016/j.plantsci.2019.02.008 https://doi.org/10.1016/j.plantsci.2019.02.008 .
Li Y G , Cui D D , Zhuo P L et al . 2019 . A new approach to promote astaxanthin accumulation via Na 2 WO 4 in Haematococcus pluvialis . Journal of Oceanology and Limnology , 37 ( 1 ): 176 - 185 , https://doi.org/10.1007/s00343-018-7317-0 https://doi.org/10.1007/s00343-018-7317-0 .
Lim K C , Yusoff F M , Shariff M et al . 2018 . Astaxanthin as feed supplement in aquatic animals . Reviews in Aquaculture , 10 ( 3 ): 738 - 773 , https://doi.org/10.1111/raq.12200 https://doi.org/10.1111/raq.12200 . https://do 10.1111/raq.12200 http://dx.doi.org/10.1111/raq.12200
Liu Y H , Alimujiang A , Wang X et al . 2019 . Ethanol induced jasmonate pathway promotes astaxanthinhyper accumulation in Haematococcus pluvialis . Bioresource Technology , 289 : 121720 , https://doi.org/10.1016/j.biortech.2019.121720 https://doi.org/10.1016/j.biortech.2019.121720 .
Luo Q L , Bian C , Tao M et al . 2019 . Genome and transcriptome sequencing of the astaxanthin-producing green microalga, Haematococcus pluvialis . Genome Biology and Evolution , 11 ( 1 ): 166 - 173 , https://doi.org/10.1093/gbe/evy263 https://doi.org/10.1093/gbe/evy263 .
Lv H X , Xia F , Liu M et al . 2016 . Metabolomic profiling of the astaxanthin accumulation process induced by high light in Haematococcus pluvialis . Algal Research , 20 : 35 - 43 , https://doi.org/10.1016/j.algal.2016.09.019 https://doi.org/10.1016/j.algal.2016.09.019 .
Naguib Y . 2000 . Antioxidant activities of astaxanthin and related carotenoids . Journal of Agricultural and Food Chemistry , 48 ( 4 ): 1150 - 1154 , https://doi.org/10.1021/jf991106k https://doi.org/10.1021/jf991106k .
Panis G , Carreon J R . 2016 . Commercial astaxanthin production derived by green alga Haematococcus pluvialis : a microalgae process model and a techno-economic assessment all through production line . Algal Research , 18 : 175 - 190 , https://doi.org/10.1016/j.algal.2016.06.007 https://doi.org/10.1016/j.algal.2016.06.007 .
Recht L , Töpfer N , Batushansky A et al . 2014 . Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis . Journal of Biological Chemistry , 289 ( 44 ): 30387 - 30403 , https://doi.org/10.1074/jbc.M114.555144 https://doi.org/10.1074/jbc.M114.555144 .
Roth MS , Cokus S J , Gallaher SD et al . 2017 . Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production . Proceedings of the National Academy of Sciences of the United States of America , 114 ( 21 ): E4296 - E4305 , https://doi.org/10.1073/pnas.1619928114 https://doi.org/10.1073/pnas.1619928114 .
Shah MMR , Liang Y M , Cheng J J et al . 2016 . Astaxanthin-producing green microalga Haematococcus pluvialis : from single cell to high value commercial products . Frontiers in Plant Science , 7 : 531 , https://doi.org/10.3389/fpls.2016.00531 https://doi.org/10.3389/fpls.2016.00531 .
Shang MM , Ding W , Zhao Y T et al . 2016 . Enhanced astaxanthin production from Haematococcus pluvialis using butylatedhydroxyanisole . Journal of Biotechnology , 236 : 199 - 207 , https://doi.org/10.1016/j.jbiotec.2016.08.019 https://doi.org/10.1016/j.jbiotec.2016.08.019 .
Su Y X , Wang J X , Shi M L et al . 2014 . Metabolomic and network analysis of astaxanthin-producing Haematococcus pluvialis under various stress conditions . Bioresource Technology , 170 : 522 - 529 , https://doi.org/10.1016/j.biortech.2014.08.018 https://doi.org/10.1016/j.biortech.2014.08.018 .
Wang X X , Huang B Q , Zhang H . 2014 . Phosphorus deficiency affects multiple macromolecular biosynthesis pathways of Thalassiosira weissflogii . Acta Oceanologica Sinica , 33 ( 4 ): 85 - 91 , https://doi.org/10.1007/s13131-014-0413-x https://doi.org/10.1007/s13131-014-0413-x .
Wells M L , Potin P , Craigie J S et al . 2017 . Algae as nutritional and functional food sources: revisiting our understanding . Journal of Applied Phycology , 29 ( 2 ): 949 - 982 , https://doi.org/10.1007/s10811-016-0974-5 https://doi.org/10.1007/s10811-016-0974-5 .
Xia S , Wan L L , Li A F et al . 2013 . Effects of nutrients and light intensity on the growth and biochemical composition of a marine microalga Odontella aurita . Chinese Journal of Oceanology and Limnology , 31 ( 6 ): 1163 - 1173 , https://doi.org/10.1007/s00343-013-2092-4 https://doi.org/10.1007/s00343-013-2092-4 .
Zhang A H , Sun H , Wang P et al . 2012 . Modern analytical techniques in metabolomics analysis . The Analyst , 137 ( 2 ): 293 - 300 , https://doi.org/10.1039/C1AN15605E https://doi.org/10.1039/C1AN15605E .
Zhang C H , Liu J G , Zhang L T . 2017 . Cell cycles and proliferation patter ns in Haematococcus pluvialis . Chinese Journal of Oceanology and Limnology , 35 ( 5 ): 1205 - 1211 , https://doi.org/10.1007/s00343-017-6103-8 https://doi.org/10.1007/s00343-017-6103-8 .
Zhang W H , Gao J W , Zhou W L et al . 2020 . Transcriptome-based analysis of Euglena gracilis lipid metabolic pathways under light stress . Turkish Journal of Fisheries and Aquatic Science , 20 ( 6 ): 453 - 465 , https://doi.org/10.4194/1303-2712-v20_6_04 https://doi.org/10.4194/1303-2712-v20_6_04 .
Zhao Y T , Yue C C , Ding W et al . 2018 . Butylatedhydroxytoluene induces astaxanthin and lipid production in Haematococcus pluvialis under high-light and nitrogen-deficiency conditions . Bioresource Technology , 266 : 315 - 321 , https://doi.org/10.1016/j.biortech.2018.06.111 https://doi.org/10.1016/j.biortech.2018.06.111 .
0
Views
0
Downloads
0
CSCD
Publicity Resources
Related Articles
Related Author
Related Institution
京公网安备11010802024621