The effects of elevated CO₂ concentrations on changes in fatty acids and amino acids of three species of microalgae

References

• Ab Lah R., Kelaher B.P., Bucher D. & Benkendorff K. 2018. Ocean warming and acidification affect the nutritional quality of the commercially-harvested turbinid snail Turbo militaris. Marine Environmental Research 141: 100–108. DOI: 10.1016/j.marenvres.2018.08.009.
   Web of Science ®Google Scholar
• Abd El Baky H.H., El-Baroty G.S. & Bouaid A. 2014. Lipid induction in Dunaliella salina culture aerated with various levels CO2 and its biodiesel production. Journal of Aquaculture Research and Development 5: 1–6. DOI: 10.4172/2155-9546.1000223.
   Google Scholar
• Abidi S.F. & Khan M.A. 2004. Dietary valine requirement of Indian major carp, Labeo rohita (Hamilton) fry. Journal of Applied Ichthyology 20: 118–122. DOI: 10.1046/j.1439-0426.2003.00526.x.
   Web of Science ®Google Scholar
• Adarme-Vega T.C., Lim D.K.Y., Timmins M., Vernen F., Li Y. & Schenk P.M. 2012. Microalgal biofactories: a promising approach towards sustainable omega-3 fatty acid production. Microbial Cell Factories 11: 96. DOI: 10.1186/1475-2859-11-96.
   PubMed Web of Science ®Google Scholar
• Arudchelvam Y. & Nirmalakhandan N. 2012. Energetic optimization of algal lipid production in bubble columns: part II: evaluation of CO2 enrichment. Biomass and Bioenergy 46: 765–772. DOI: 10.1016/j.biombioe.2012.08.012.
   Web of Science ®Google Scholar
• Assunção J., Batista A.P., Manoel J., da Silva T.L., Marques P., Reis A. & Gouveia L. 2017. CO2 utilization in the production of biomass and biocompounds by three different microalgae. Engineering in Life Sciences 17: 1126–1135. DOI: 10.1002/elsc.201700075.
   Web of Science ®Google Scholar
• Ben-Amotz A., Katz A. & Avron M. 1982. Accumulation of β-carotene in halotolerant algae: purification and characterization of β-carotene-rich globules from Dunaliella bardawil (Chlorophyceae). Journal of Phycology 18: 529–537. DOI: 10.1111/j.1529-8817.1982.tb03219.x.
   Web of Science ®Google Scholar
• Bermúdez R., Feng Y., Roleda M.Y., Tatters A.O., Hutchins D.A., Larsen T., Boyd P.W., Hurd C.L., Riebesell U. & Winder M. 2015. Long-term conditioning to elevated pCO2 and warming influences the fatty and amino acid composition of the diatom Cylindrotheca fusiformis. PLOS One 10: e0123945. DOI: 10.1371/journal.pone.0123945.
   Web of Science ®Google Scholar
• Bi R., Ismar S., Sommer U. & Zhao M. 2017. Environmental dependence of the correlations between stoichiometric and fatty acid‐based indicators of phytoplankton nutritional quality. Limnology and Oceanography 62: 334–347. DOI: 10.1002/lno.10429.
   Web of Science ®Google Scholar
• Cao X., Xi Y., Liu J., Chu Y., Wu P., Yang M., Chi Z. & Xue S. 2019. New insights into the CO2-steady and pH-steady cultivations of two microalgae based on continuous online parameter monitoring. Algal Research 38: 101370. DOI: 10.1016/j.algal.2018.11.021.
   Google Scholar
• Carballo-Cárdenas E.C., Tuan P.M., Janssen M. & Wijffels R.H. 2003. Vitamin E (α -tocopherol) production by the marine microalgae Dunaliella tertiolecta and Tetraselmis suecica in batch cultivation. Biomolecular Engineering 20: 139–147. DOI: 10.1016/S1389-0344(03)00040-6.
   PubMedGoogle Scholar
• Chen B., Zou D., Zhu M. & Yang Y. 2017. Effects of CO2 levels and light intensities on growth and amino acid contents in red seaweed Gracilaria lemaneiformis. Aquaculture Research 48: 2683–2690. DOI: 10.1111/are.13100.
   Web of Science ®Google Scholar
• Chisti Y. 2008. Biodiesel from microalgae beats bioethanol. Trends in Biotechnology 26: 126–131. DOI: 10.1016/j.tibtech.2007.12.002.
   PubMed Web of Science ®Google Scholar
• Chiu S.Y., Kao C.Y., Tsai M.T., Ong S.C., Chen C.H. & Lin C.S. 2009. Lipid accumulation and CO2 utilization of Nannochloropsis oculata in response to CO2 aeration. Bioresource Technology 100: 833–838. DOI: 10.1016/j.biortech.2008.06.061.
   PubMed Web of Science ®Google Scholar
• Cooper T.F. & Ulstrup K.E. 2009. Mesoscale variation in the photophysiology of the reef building coral Pocillopora damicornis along an environmental gradient. Estuarine, Coastal and Shelf Science 83: 186–196. DOI: 10.1016/j.ecss.2009.03.015.
   Web of Science ®Google Scholar
• Cornish M.L. & Garbary D.J. 2010. Antioxidants from macroalgae: potential applications in human health and nutrition. Algae 25: 155–171. DOI: 10.4490/algae.2010.25.4.155.
   Google Scholar
• Dong H.P., Williams E., Wang D.Z., Xie Z.X., Hsia R.C., Jenck A., Halden R., Li J., Chen F. & Place A.R. 2013. Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Plant Physiology 162: 1110–1126. DOI: 10.1104/pp.113.214320.
   PubMed Web of Science ®Google Scholar
• Gao G., Clare A.S., Chatzidimitriou E., Rose C. & Caldwell G. 2018. Effects of ocean warming and acidification, combined with nutrient enrichment, on chemical composition and functional properties of Ulva rigida. Food Chemistry 258: 71–78. DOI: 10.1016/j.foodchem.2018.03.040.
   PubMed Web of Science ®Google Scholar
• Gao G., Clare A.S., Rose C. & Caldwell G.S. 2017. Reproductive sterility increases the capacity to exploit the green seaweed Ulva rigida for commercial applications. Algal Research 24: 64–71. DOI: 10.1016/j.algal.2017.03.008.
   Google Scholar
• Gao G., Gao Q., Bao M., Xu J. & Li X. 2019. Nitrogen availability modulates the effects of ocean acidification on biomass yield and food quality of a marine crop Pyropia yezoensis. Food Chemistry 271: 623–629. DOI: 10.1016/j.foodchem.2018.07.090.
   Web of Science ®Google Scholar
• García-Casal M.N., Ramírez J., Leets I., Pereira A.C. & Quiroga M.F. 2009. Antioxidant capacity, polyphenol content and iron bioavailability from algae (Ulva sp., Sargassum sp. and Porphyra sp.) in human subjects. British Journal of Nutrition 101: 79–85. DOI: 10.1017/S0007114508994757.
   PubMed Web of Science ®Google Scholar
• Glencross B.D. 2009. Exploring the nutritional demand for essential fatty acids by aquaculture species. Reviews in Aquaculture 1: 71–124. DOI: 10.1111/j.1753-5131.2009.01006.x.
   Web of Science ®Google Scholar
• Gorman D.S. & Levine R.P. 1965. Cytochrome   f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proceedings of the National Academy of Sciences of the United States of America 54: 1665–1669. DOI: 10.1073/pnas.54.6.1665.
   PubMed Web of Science ®Google Scholar
• Griffiths M.J., van Hille R.P. & Harrison S.T.L. 2014. The effect of nitrogen limitation on lipid productivity and cell composition in Chlorella vulgaris. Applied Microbiology and Biotechnology 98: 2345–2356. DOI: 10.1007/s00253-013-5442-4.
   PubMed Web of Science ®Google Scholar
• Guillard R.R.L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Culture of marine invertebrate animals (Ed. by W.L. Smith & M.H. Chanley), pp. 29–60. Plenum Press, New York, USA.
   Google Scholar
• Hu H. & Gao K. 2003. Optimization of growth and fatty acid composition of a unicellular marine picoplankton, Nannochloropsis sp., with enriched carbon sources. Biotechnology Letters 25: 421–425. DOI: 10.1023/a:1022489108980.
   PubMed Web of Science ®Google Scholar
• Hundley J.M., Ing R.B. & Krauss R.W. 1956. Algae as sources of lysine and threonine in supplementing wheat and bread diets. Science (Washington) 124: 536–537. DOI: 10.1126/science.124.3221.536.
   Web of Science ®Google Scholar
• Jahan A., Ahmad I.Z., Fatima N., Ansari V.A. & Akhtar J. 2017. Algal bioactive compounds in the cosmeceutical industry: a review. Phycologia 56: 410–422. DOI: 10.2216/15.58.1.
   Web of Science ®Google Scholar
• Ji M.K., Yun H.S., Hwang J.H., Salama E.S., Jeon B.H. & Choi J. 2017. Effect of flue gas CO2 on the growth, carbohydrate and fatty acid composition of a green microalga Scenedesmus obliquus for biofuel production. Environmental Technology 38: 2085–2092. DOI: 10.1080/09593330.2016.1246145.
   PubMed Web of Science ®Google Scholar
• Kim K., Hoh D., Ji Y., Do H., Lee B. & Holzapfel W. 2013. Impact of light intensity, CO2 concentration and bubble size on growth and fatty acid composition of Arthrospira (Spirulina) platensis KMMCC CY-007. Biomass and Bioenergy 49: 181–187. DOI: 10.1016/j.biombioe.2012.12.021.
   Web of Science ®Google Scholar
• Kim M.S., Baek J.S., Yun Y.S., Sim S.J., Park S. & Kim S.C. 2006. Hydrogen production from Chlamydomonas reinhardtii biomass using a two-step conversion process: anaerobic conversion and photosynthetic fermentation. International Journal of Hydrogen Energy 31: 812–816. DOI: 10.1016/j.ijhydene.2005.06.009.
   Web of Science ®Google Scholar
• Kinsella J.E., Lokesh B. & Stone R.A. 1990. Dietary n-3 polyunsaturated fatty acids and amelioration of cardiovascular disease: possible mechanisms. The American Journal of Clinical Nutrition 52: 1–28. DOI: 10.1093/ajcn/52.1.1.
   PubMed Web of Science ®Google Scholar
• Kumar A., AbdElgawad H., Castellano I., Selim S., Beemster G.T.S., Han A., Buia M.C. & Palumbo A. 2018. Effects of ocean acidification on the levels of primary and secondary metabolites in the brown macroalga Sargassum vulgare at different time scales. Science of the Total Environment 643: 946–956. DOI: 10.1016/j.scitotenv.2018.06.176.
   Web of Science ®Google Scholar
• Lalibertè G. & de la Noüe J. 1993. Auto-, hetero-, and mixotrophic growth of Chlamydomonas humicola (Cmloroimiyckak) on acetate. Journal of Phycology 29: 612–620. DOI: 10.1111/j.0022-3646.1993.00612.x.
   Web of Science ®Google Scholar
• Landymore A.F. & Antia N.J. 1977. Growth of a marine diatom and a haptophycean alga on phenylalanine or tyrosine serving as sole nitrogen source. Journal of Phycology 13: 231–238. DOI: 10.1111/j.1529-8817.1977.tb02921.x.
   Web of Science ®Google Scholar
• Li Z., Meng T., Ling X., Li J., Zheng C., Shi Y., Chen Z., Li Z., Li Q., Lu Y. & He N. 2018. Overexpression of malonyl-CoA: ACP transacylase in Schizochytrium sp. to improve polyunsaturated fatty acid production. Journal of Agricultural and Food Chemistry 66: 5382–5391. DOI: 10.1021/acs.jafc.8b01026.
   PubMed Web of Science ®Google Scholar
• Liu J., Liu Y., Wang H. & Xue S. 2015. Direct transesterification of fresh microalgal cells. Bioresource Technology 176: 284–287. DOI: 10.1016/j.biortech.2014.10.094.
   PubMed Web of Science ®Google Scholar
• Meng Y., Jiang J., Wang H., Cao X., Xue S., Yang Q. & Wang W. 2015. The characteristics of TAG and EPA accumulation in Nannochloropsis oceanica IMET1 under different nitrogen supply regimes. Bioresource Technology 179: 483–489. DOI: 10.1016/j.biortech.2014.12.012.
   PubMed Web of Science ®Google Scholar
• Moreno R., Aita G.M., Madsen L., Gutierrez D.L., Yao S., Hurlburt B. & Brashear S. 2013. Identification of naturally isolated southern Louisiana’s algal strains and the effect of higher CO2 content on fatty acid profiles for biodiesel production. Journal of Chemical Technology and Biotechnology 88: 948–957. DOI: 10.1002/jctb.3930.
   Web of Science ®Google Scholar
• Mudimu O., Rybalka N., Bauersachs T., Friedl T. & Schulz R. 2015. Influence of different CO2 concentrations on microalgae growth, α-tocopherol content and fatty acid composition. Geomicrobiology Journal 32: 291–303. DOI: 10.1080/01490451.2014.889784.
   Web of Science ®Google Scholar
• Müller-Navarra D.C., Brett M.T., Park S., Chandra S., Ballantyne A.P., Zorita E. & Goldman C.R. 2004. Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes. Nature (London) 427: 69–72. DOI: 10.1038/nature02210.
   PubMed Web of Science ®Google Scholar
• Murthy K.N.C., Vanitha A., Rajesha J., Swamy M.M., Sowmya P.R. & Ravishankar G.A. 2005. In vivo antioxidant activity of carotenoids from Dunaliella salina—a green microalga. Life Sciences 76: 1381–1390. DOI: 10.1016/j.lfs.2004.10.015.
   PubMed Web of Science ®Google Scholar
• Nakanishi A., Aikawa S., Ho S.H., Chen C.Y., Chang J.S., Hasunuma T. & Kondo A. 2014. Development of lipid productivities under different CO2 conditions of marine microalgae Chlamydomonas sp. JSC4. Bioresource Technology 152: 247–252. DOI: 10.1016/j.biortech.2013.11.009.
   Web of Science ®Google Scholar
• Ota M., Kato Y., Watanabe H., Watanabe M., Sato Y., Smith R.L. Jr. & Inomata H. 2009. Fatty acid production from a highly CO2 tolerant alga, Chlorocuccum littorale, in the presence of inorganic carbon and nitrate. Bioresource Technology 100: 5237–5242. DOI: 10.1016/j.biortech.2009.05.048.
   PubMed Web of Science ®Google Scholar
• Recht L., Zarka A. & Boussiba S. 2012. Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Applied Microbiology and Biotechnology 94: 1495–1503. DOI: 10.1007/s00253-012-3940-4.
   PubMed Web of Science ®Google Scholar
• Ren M., Ogden K. & Lian B. 2013. Effect of culture conditions on the growth rate and lipid production of microalgae Nannochloropsis gaditana. Journal of Renewable and Sustainable Energy 5: 063138. DOI: 10.1063/1.4857375.
   Web of Science ®Google Scholar
• Renberg L., Johansson A.I., Shutova T., Stenlund H., Aksmann A., Raven J.A., Gardeström P., Moritz T. & Samuelsson G. 2010. A metabolomic approach to study major metabolite changes during acclimation to limiting CO2 in Chlamydomonas reinhardtii. Plant Physiology 154: 187–196. DOI: 10.1104/pp.110.157651.
   PubMed Web of Science ®Google Scholar
• Riazi R., Rafii M., Wykes L.J., Ball R.O. & Pencharz P.B. 2003. Valine may be the first limiting branched-chain amino acid in egg protein in men. The Journal of Nutrition 133: 3533–3539. DOI: 10.1093/jn/133.11.3533.
   Web of Science ®Google Scholar
• Riebesell U., Revill A.T., Holdsworth D.G. & Volkman J.K. 2000. The effects of varying CO2 concentration on lipid composition and carbon isotope fractionation in Emiliania huxleyi. Geochimica et Cosmochimica Acta 64: 4179–4192. DOI: 10.1016/S0016-7037(00)00474-9.
   Web of Science ®Google Scholar
• Rocha J.M.S., Garcia J.E.C. & Henriques M.H.F. 2003. Growth aspects of the marine microalga Nannochloropsis gaditana. Biomolecular Engineering 20: 237–242. DOI: 10.1016/S1389-0344(03)00061-3.
   PubMedGoogle Scholar
• Rossoll D., Bermúdez R., Hauss H., Schulz K.G., Riebesell U., Sommer U. & Winder M. 2012. Ocean acidification-induced food quality deterioration constrains trophic transfer. PLOS One 7: e34737. DOI: 10.1371/journal.pone.0034737.
   Web of Science ®Google Scholar
• Sato N., Tsuzuki M. & Kawaguchi A. 2003. Glycerolipid synthesis in Chlorella kessleri 11 h: II. Effect of the CO2 concentration during growth. Biochimica et Biophysica Acta (BBA)-molecular and Cell Biology of Lipids 1633: 35–42. DOI: 10.1016/S1388-1981(03)00070-2.
   Web of Science ®Google Scholar
• Schmitz G. & Ecker J. 2008. The opposing effects of n−3 and n−6 fatty acids. Progress in Lipid Research 47: 147–155. DOI: 10.1016/j.plipres.2007.12.004.
   PubMed Web of Science ®Google Scholar
• Senhorinho G.N.A., Ross G.M. & Scott J.A. 2015. Cyanobacteria and eukaryotic microalgae as potential sources of antibiotics. Phycologia 54: 271–282. DOI: 10.2216/14-092.1.
   Web of Science ®Google Scholar
• Spolaore P., Joannis-Cassan C., Duran E. & Isambert A. 2006. Commercial applications of microalgae. Journal of Bioscience and Bioengineering 101: 87–96. DOI: 10.1263/jbb.101.87.
   PubMed Web of Science ®Google Scholar
• Stansell G.R., Gray V.M. & Sym S.D. 2012. Microalgal fatty acid composition: implications for biodiesel quality. Journal of Applied Phycology 24: 791–801. DOI: 10.1007/s10811-011-9696-x.
   Web of Science ®Google Scholar
• Tang D., Han W., Li P., Miao X. & Zhong J. 2011a. CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresource Technology 102: 3071–3076. DOI: 10.1016/j.biortech.2010.10.047.
   PubMed Web of Science ®Google Scholar
• Tang H., Abunasser N., Garcia M.E.D., Chen M., Ng K.Y.S. & Salley S.O. 2011b. Potential of microalgae oil from Dunaliella tertiolecta as a feedstock for biodiesel. Applied Energy 88: 3324–3330. DOI: 10.1016/j.apenergy.2010.09.013.
   Web of Science ®Google Scholar
• Torstensson A., Hedblom M., Mattsdotter Björk M., Chierici M. & Wulff A. 2015. Long-term acclimation to elevated pCO2 alters carbon metabolism and reduces growth in the Antarctic diatom Nitzschia lecointei. Proceedings of the Royal Society B: Biological Sciences 282: 20151513. DOI: 10.1098/rspb.2015.1513.
   Web of Science ®Google Scholar
• Valfré F., Caprino F. & Turchini G.M. 2003. The health benefit of seafood. Veterinary Research Communications 27: 507–512. DOI: 10.1023/B:VERC.0000014208.47984.8c.
   PubMed Web of Science ®Google Scholar
• Vance P. & Spalding M.H. 2005. Growth, photosynthesis, and gene expression in Chlamydomonas over a range of CO2 concentrations and CO2/O2 ratios: CO2 regulates multiple acclimation states. Canadian Journal of Botany 83: 796–809. DOI: 10.1139/b05-064.
   Google Scholar
• Wahbeh M.I. 1997. Amino acid and fatty acid profiles of four species of macroalgae from Aqaba and their suitability for use in fish diets. Aquaculture 159: 101–109. DOI: 10.1016/S0044-8486(97)00183-X.
   Web of Science ®Google Scholar