Biochemical composition of the brown tide causative species <i>Aureococcus anophagefferens</i> cultivated in different nitrogen sources -- Journal of Oceanology and Limnology,2022,40(6):2189-2201

	Cite this paper:
	Jian GAO, Yuelei DONG, Xiaoyu ZHOU, Lei CUI, Songhui LÜ. Biochemical composition of the brown tide causative species Aureococcus anophagefferens cultivated in different nitrogen sources[J]. Journal of Oceanology and Limnology, 2022, 40(6): 2189-2201

Biochemical composition of the brown tide causative species Aureococcus anophagefferens cultivated in different nitrogen sources

Jian GAO¹, Yuelei DONG^1,3, Xiaoyu ZHOU¹, Lei CUI^1,3, Songhui LÜ^1,2,3

1 Research Center of Harmful Algae and Marine Biology, College of Life Science and Technology, Jinan University, Guangzhou 510632, China;
2 Southern Marine Science and Engineering Guangdong Laboratory, Zhuhai 519000, China;
3 Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China

Abstract:

A large-scale algal bloom, caused by Aureococcus anophagefferens, has plagued the coastal embayment of Qinhuangdao, China since 2009. The bay scallop agriculture industry in this area has been adversely affected. Researchers claimed that the poor nutritional value of brown tide cells might be responsible for the detrimental effects on bivalve mollusks. To verify whether brown tide cells are nutritionally inadequate food sources, the biochemical composition (total extractable lipids, amino acids, fatty acids, and monomeric carbohydrates) of the Chinese strain A. anophagefferens was determined during the late logarithmic growth phase when culturing in different nitrogen sources (nitrate, urea and nitrate-urea mixture). Cells cultured in nitrate contained 39.12% protein, 21.99% total extractable lipid, 10.25% total carbohydrates, and a relatively high amount of polyunsaturated fatty acid (PUFA) (51.98%, percentage of total fatty acids), including eicosapentaenoic acid (EPA) (4.81%) and docosahexaenoic acid (DHA) (14.56%). The gross biochemical composition and PUFA content in A. anophagefferens in nitrate cultivation are comparable with values found in the literature of frequently used species in bivalve feeding. Nine monomeric carbohydrates were significantly reduced when cultivated in urea and nitrate-urea mixture (P<0.05). The DHA, EPA, and PUFA contents significantly decreased when cultivated in urea (P<0.05). Although the nutritional value of A. anophagefferens dropped when cultured in urea, it is still comparable with certain favorably used algal species in bivalve feeding (i.e., Skeletonema costatum), indicating that A. anophagefferens is not a nutritionally inadequate food source.

Key words: brown tide|Aureococcus anophagefferens|fatty acid|carbohydrate|nutritional value

Received: 2021-10-18 Revised:

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References:
Bigelow N, Barker J, Ryken S et al. 2013. Chrysochromulina sp.: a proposed lipid standard for the algal biofuel industry and its application to diverse taxa for screening lipid content. Algal Research, 2(4): 385-393, https://doi.org/10.1016/j.algal.2013.07.001.
Bligh E G, Dyer W J. 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8): 911-917, https://doi.org/10.1139/o59-099.
Bricelj V M, Fisher N S, Guckert J B et al. 1989. Lipid composition and nutritional value of the brown tide alga Aureococcus anophagefferens. In: Cosper E M, Bricelj V M, Carpenter E J eds. Novel Phytoplankton Blooms.Springer, Berlin. p.85-100.
Bricelj V M, Kuenstner S H. 1989. Effects of the “brown tide” on the feeding physiology and growth of bay scallops and mussels. In: Cosper E M, Bricelj V M, Carpenter E J eds.Novel Phytoplankton Blooms. Springer, Berlin. p.491-509.
Bricelj V M, Lonsdale D J. 1997. Aureococcus anophagefferens:causes and ecological consequences of brown tides in U.S. mid‐Atlantic coastal waters. Limnology and Oceanography, 42(5 Pt 2): 1023-1038, https://doi.org/10. 4319/lo.1997.42.5_part_2.1023.
Bricelj V M, MacQuarrie S P, Smolowitz R. 2004.Concentration-dependent effects of toxic and nontoxic isolates of the brown tide alga Aureococcus anophagefferens on growth of juvenile bivalves. Marine Ecology Progress Series, 282: 101-114, https://doi.org/10.3354/meps282101.
Bricelj V M, MacQuarrie S P. 2007. Effects of brown tide(Aureococcus anophagefferens) on hard clam Mercenaria mercenaria larvae and implications for benthic recruitment. Marine Ecology Progress Series, 331: 147-159, https://doi.org/10.3354/meps331147.
Bricelj V, MacQuarrie S, Schaffner R. 2001. Differential effects of Aureococcus anophagefferens isolates (“brown tide”) in unialgal and mixed suspensions on bivalve feeding. Marine Biology, 139(4): 605-616, https://doi.org/10.1007/s002270100612.
Brown M R. 1991. The amino-acid and sugar composition of 16 species of microalgae used in mariculture. Journal of Experimental Marine Biology and Ecology, 145(1): 79-99, https://doi.org/10.1016/0022-0981(91)90007-J.
Brown M R. 2002. Nutritional value and use of microalgae in aquaculture. In: Cruz-Suárez L E, Ricque-Marie D, TapiaSalazar M et al. eds. Avances en Nutrición Acuicola VI.Memorias del VI Simposium Internacional de Nutrición Acuícola. Cancún.
Caron D A, Gobler C J, Lonsdale D J et al. 2004. Microbial herbivory on the brown tide alga, Aureococcus anophagefferens: results from natural ecosystems, mesocosms and laboratory experiments. Harmful Algae, 3(4): 439-457, https://doi.org/10.1016/j.hal.2004.06.011.
Cavanaugh G M. 1956. Formulae and Methods IV of the Marine Biological Laboratory Chemical Room. Marine Biological Laboratory, Woods Hole. p.67-69.
Cheng P F, Zhou C X, Chu R R et al. 2020. Effect of microalgae diet and culture system on the rearing of bivalve mollusks:nutritional properties and potential cost improvements.Algal Research, 51: 102076, https://doi.org/10.1016/j.algal.2020.102076.
Cranford P J. 2019. Magnitude and extent of water clarification services provided by bivalve suspension feeding. In:Smaal A C, Ferreira J G, Grant J et al. eds. Goods and Services of Marine Bivalves. Springer, Cham. p.119-141.
Da Costa F, Robert R, Quéré C et al. 2015. Essential fatty acid assimilation and synthesis in larvae of the bivalve Crassostrea gigas. Lipids, 50(5): 503-511, https://doi.org/10.1007/s11745-015-4006-z.
Delaporte M, Chu F L, Langdon C et al. 2007. Changes in biochemical and hemocyte parameters of the Pacific oysters Crassostrea gigas fed T-ISO supplemented with lipid emulsions rich in eicosapentaenoic acid. Journal of Experimental Marine Biology and Ecology, 343(2): 261-275, https://doi.org/10.1016/j.jembe.2006.12.021.
Delaunay F, Marty Y, Moal J et al. 1993. The effect of monospecific algal diets on growth and fatty acid composition of Pecten maximus (L.) larvae. Journal of Experimental Marine Biology and Ecology, 173(2): 163-179, https://doi.org/10.1016/0022-0981(93)90051-O.
Dong H P, Huang K X, Wang H L et al. 2014. Understanding strategy of nitrate and urea assimilation in a Chinese strain of Aureococcus anophagefferens through RNASeq analysis. PLoS One, 9(10): e111069, https://doi.org/10.1371/journal.pone.0111069.
Durmaz Y. 2007. Vitamin E (α-tocopherol) production by the marine microalgae Nannochloropsis oculata(Eustigmatophyceae) in nitrogen limitation. Aquaculture, 272(1-4): 717-722, https://doi.org/10.1016/j.aquaculture. 2007.07.213.
Fernández-Reiriz M J, Pérez-Camacho A, Peteiro L G et al. 2011. Growth and kinetics of lipids and fatty acids of the clam Venerupis pullastra during larval development and postlarvae. Aquaculture Nutrition, 17(1): 13-23, https://doi.org/10.1111/j.1365-2095.2009.00701.x.
Gainey Jr L F, Shumway S E. 1991. The physiological effect of Aureococcus anophagefferens (“brown tide”) on the lateral cilia of bivalve mollusks. The Biological Bulletin, 181(2): 298-306, https://doi.org/10.2307/1542101.
Gallager S M, Stoecker D K, Bricelj V M. 1989. Effects of the brown tide alga on growth, feeding physiology and locomotory behavior of scallop larvae (Argopecten irradians). In: Cosper E M, Bricelj V M, Carpenter EJ eds. Novel Phytoplankton Blooms. Springer, Berlin.p.511-541.
Gobler C J, Sunda W G. 2012. Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis. Harmful Algae, 14: 36-45, https://doi.org/10.1016/j.hal.2011.10.013.
Greenfield D I, Lonsdale D J, Cerrato R M et al. 2004.Effects of background concentrations of Aureococcus anophagefferens (brown tide) on growth and feeding in the bivalve Mercenaria mercenaria. Marine Ecology Progress Series, 274: 171-181, https://doi.org/10.3354/meps274171.
Griffith A W, Harke M J, DePasquale E et al. 2019. The harmful algae, Cochlodinium polykrikoides and Aureococcus anophagefferens, elicit stronger transcriptomic and mortality response in larval bivalves (Argopecten irradians) than climate change stressors. Ecology and Evolution, 9(8):4931-4948, https://doi.org/10.1002/ece3.5100.
Guedes A C, Malcata F X. 2012. Nutritional value and uses of microalgae in aquaculture. In: Muchlisin Z ed.Aquaculture. IntechOpen. p.59-78.
Guillard R R L, Ryther J H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology, 8(2): 229-239.
Harke M J, Gobler C J, Shumway S E. 2011. Suspension feeding by the Atlantic slipper limpet (Crepidula fornicata) and the northern quahog (Mercenaria mercenaria) in the presence of cultured and wild populations of the harmful brown tide alga, Aureococcus anophagefferens.Harmful Algae, 10(5): 503-511, https://doi.org/10.1016/j.hal.2011.03.005.
He X J, Han D D, Han L Y et al. 2018. Grazing and performance of the copepod Pseudodiaptomus poplesia on a Chinese strain of Aureococcus anophagefferens. Acta Oceanologica Sinica, 37(4): 69-76, https://doi.org/10.1007/s13131-018-1168-6.
Helm M M, Laing I. 1987. Preliminary observations on the nutritional value of ‘Tahiti Isochrysis’ to bivalve larvae. Aquaculture, 62(3-4): 281-288, https://doi.org/10.1016/0044-8486(87)90170-0.
Hemaiswarya S, Raja R, Kumar R R et al. 2011. Microalgae:a sustainable feed source for aquaculture. World Journal of Microbiology and Biotechnology, 27(8): 1737-1746, https://doi.org/10.1007/s11274-010-0632-z.
Jónasdóttir S H. 2019. Fatty acid profiles and production in marine phytoplankton. Marine Drugs, 17(3): 151, https://doi.org/10.3390/md17030151.
Kana T M, Lomas M W, MacIntyre H L et al. 2004.Stimulation of the brown tide organism, Aureococcus anophagefferens, by selective nutrient additions to in situ mesocosms. Harmful Algae, 3(4): 377-388, https://doi.org/10.1016/j.hal.2004.06.008.
Kaparapu J. 2018. Application of microalgae in aquaculture.Phykos, 48(1): 21-26.
Keller A A, Rice R L. 1989. Effects of nutrient enrichment on natural populations of the brown tide phytoplankton Aureococcus anophagefferens (Chrysophyceae). Journal of Phycology, 25(4): 636-646, https://doi.org/10.1111/j.0022-3646.1989.00636.x.
Knauer J, Southgate P C. 1999. A review of the nutritional requirements of bivalves and the development of alternative and artificial diets for bivalve aquaculture.Reviews in Fisheries Science, 7(3-4): 241-280, https://doi.org/10.1080/10641269908951362.
Langdon C J, Waldock M J. 1981. The effect of algal and artificial diets on the growth and fatty acid composition of Crassostrea gigas spat. Journal of the Marine Biological Association of the United Kingdom, 61(2): 431-448, https://doi.org/10.1017/S0025315400047056.
Laurens L M L. 2016. Summative Mass Analysis of Algal Biomass-Integration of Analytical Procedures: Laboratory Analytical Procedure (LAP). National Renewable Energy Lab. (NREL), Golden, CO, USA.
Leonardos N, Lucas I A N. 2000. The nutritional value of algae grown under different culture conditions for Mytilus edulis L. larvae. Aquaculture, 182(3-4): 301-315, https://doi.org/10.1016/S0044-8486(99)00269-0.
Levasseur M, Thompson P A, Harrison P J. 1993. Physiological acclimation of marine phytoplankton to different nitrogen sources. Journal of Phycology, 29(5): 587-595, https://doi.org/10.1111/j.0022-3646.1993.00587.x.
Liu H B, Buskey E J. 2000. The exopolymer secretions (EPS) layer surrounding Aureoumbra lagunensis cells affects growth, grazing, and behavior of protozoa. Limnology and Oceanography, 45(5): 1187-1191, https://doi.org/10.4319/lo.2000.45.5.1187.
Lonsdale D J, Cosper E M, Kim W S et al. 1996. Food web interactions in the plankton of Long Island bays, with preliminary observations on brown tide effects. Marine Ecology Progress Series, 134: 247-263, https://doi.org/10.3354/meps134247.
Lourenco S O, Barbarino E, Mancini-Filho J et al. 2002.Effects of different nitrogen sources on the growth and biochemical profile of 10 marine microalgae in batch culture: an evaluation for aquaculture. Phycologia, 41(2):158-168, https://doi.org/10.2216/i0031-8884-41-2-158.1.
Marshall R, McKinley S, Pearce C M. 2010. Effects of nutrition on larval growth and survival in bivalves. Reviews in Aquaculture, 2(1): 33-55, https://doi.org/10.1111/j.1753-5131.2010.01022.x.
Martínez-Fernández E, Acosta-Salmón H, Southgate P C. 2006. The nutritional value of seven species of tropical microalgae for black-lip pearl oyster (Pinctada margaritifera, L.) larvae. Aquaculture, 257(1-4): 491-503, https://doi.org/10.1016/j.aquaculture.2006.03.022.
Matias D, Joaquim S, Ramos M et al. 2011. Biochemical compounds’ dynamics during larval development of the carpet-shell clam Ruditapes decussatus (Linnaeus, 1758): effects of mono-specific diets and starvation.Helgoland Marine Research, 65(3): 369-379, https://doi.org/10.1007/s10152-010-0230-3.
Milke L M, Bricelj V M, Parrish C C. 2006. Comparison of early life history stages of the bay scallop, Argopecten irradians: effects of microalgal diets on growth and biochemical composition. Aquaculture, 260(1-4): 272-289, https://doi.org/10.1016/j.aquaculture.2006.06.004.
Milke L M, Bricelj V M, Parrish C C. 2008. Biochemical characterization and nutritional value of three Pavlova spp. in unialgal and mixed diets with Chaetoceros muelleri for postlarval sea scallops, Placopecten magellanicus. Aquaculture, 276(1-4): 130-142, https://doi.org/10.1016/j.aquaculture.2008.01.040.
Mulholland M R, Boneillo G E, Bernhardt P W et al. 2009.Comparison of nutrient and microbial dynamics over a seasonal cycle in a mid-Atlantic coastal lagoon prone to Aureococcus anophagefferens (brown tide) blooms.Estuaries and Coasts, 32(6): 1176-1194, https://doi.org/10.1007/s12237-009-9218-0.
Ou L J, Cai Y Y, Jin W Y et al. 2018a. Understanding the nitrogen uptake and assimilation of the Chinese strain of Aureococcus anophagefferens (Pelagophyceae).Algal Research, 34: 182-190, https://doi.org/10.1016/j.algal.2018.07.019.
Ou L J, Liu X H, Li J J et al. 2018b. Significant activities of extracellular enzymes from a brown tide in the coastal waters of Qinhuangdao, China. Harmful Algae, 74: 1-9, https://doi.org/10.1016/j.hal.2018.03.005.
Padilla D K, Doall M H, Gobler C J et al. 2006. Brown tide alga, Aureococcus anophagefferens, can affect growth but not survivorship of Mercenaria mercenaria larvae.Harmful Algae, 5(6): 736-748, https://doi.org/10.1016/j.hal.2006.03.004.
Portilla S E, Branco B F, Tanacredi J T. 2015. Preliminary investigation into the effects of two dietary fatty acids, 20:5n-3 and 22:6n-3, on mortality of juvenile Mercenaria mercenaria during the approach to winter. Aquaculture International, 23(6): 1357-1376, https://doi.org/10.1007/s10499-015-9889-4.
Probyn T A, Bernard S, Pitcher G C et al. 2010. Ecophysiological studies on Aureococcus anophagefferens blooms in Saldanha Bay, South Africa. Harmful Algae, 9(2): 123-133, https://doi.org/10.1016/j.hal.2009.08.008.
Probyn T, Pitcher G, Pienaar R et al. 2001. Brown tides and mariculture in Saldanha bay, South Africa.Marine Pollution Bulletin, 42(5): 405-408, https://doi.org/10.1016/S0025-326X(00)00170-3.
Saucedo P E, González-Jiménez A, Acosta-Salmón H et al. 2013. Nutritional value of microalgae-based diets for lionspaw scallop (Nodipecten subnodosus) juveniles reared at different temperatures. Aquaculture, 392-395: 113-119, https://doi.org/10.1016/j.aquaculture.2013.02.001.
Sieburth J M, Johnson P W, Hargraves P E. 1988. Ultrastructure and ecology of Aureococcus anophageferens gen. et sp.nov. (Chrysophyceae): the Dominant picoplankter during a bloom in Narragansett bay, Rhode Island, summer 1985. Journal of Phycology, 24(3): 416-425, https://doi.org/10.1111/j.1529-8817.1988.tb04485.x.
Smith J K, Lonsdale D J, Gobler C J et al. 2008. Feeding behavior and development of Acartia tonsa nauplii on the brown tide alga Aureococcus anophagefferens.Journal of Plankton Research, 30(8): 937-950, https://doi.org/10.1093/plankt/fbn050.
Tang B J, Liu B Z, Wang G D et al. 2006. Effects of various algal diets and starvation on larval growth and survival of Meretrix meretrix. Aquaculture, 254(1-4): 526-533, https://doi.org/10.1016/j.aquaculture.2005.11.012.
Tracey G A. 1988. Feeding reduction, reproductive failure, and mortality in Mytilus edulis during the 1985 ‘brown tide’ in Narragansett Bay, Rhode Island. Marine Ecology Progress Series, 50: 73-81.
Uriarte I, Farı́as A. 1999. The effect of dietary protein content on growth and biochemical composition of Chilean scallop Argopecten purpuratus (L.) postlarvae and spat.Aquaculture, 180(1-2): 119-127, https://doi.org/10.1016/S0044-8486(99)00145-3.
Van Houcke J, Medina I, Maehre H K et al. 2017. The effect of algae diets (Skeletonema costatum and Rhodomonas baltica) on the biochemical composition and sensory characteristics of Pacific cupped oysters(Crassostrea gigas) during land-based refinement. Food Research International, 100(Pt 1): 151-160, https://doi.org/10.1016/j.foodres.2017.06.041.
Van Wychen S, Laurens L M L. 2016. Determination of Total Solids and Ash in Algal Biomass: Laboratory Analytical Procedure (LAP). National Renewable Energy Lab.(NREL), Golden, CO, USA.
Van Wychen S, Laurens L M L. 2020. Total carbohydrate content determination of microalgal biomass by acid hydrolysis followed by spectrophotometry or liquid chromatography. In: Spilling K ed. Biofuels from Algae:Methods and Protocols. Humana, New York. p.191-202, https://doi.org/10.1007/7651_2017_106.
Van Wychen S, Ramirez K, Laurens L M L. 2016.Determination of Total Lipids as Fatty Acid Methyl Esters (FAME) by in Situ Transesterification: Laboratory Analytical Procedure (LAP). National Renewable Energy Lab. (NREL), Golden, CO, USA.
Volkman J K, Jeffrey S W, Nichols P D et al. 1989. Fatty acid and lipid composition of 10 species of microalgae used in mariculture. Journal of Experimental Marine Biology and Ecology, 128(3): 219-240, https://doi.org/10.1016/0022-0981(89)90029-4.
Wikfors G H, Ferris G E, Smith B C. 1992. The relationship between gross biochemical composition of cultured algal foods and growth of the hard clam, Mercenaria mercenaria (L.). Aquaculture, 108(1-2): 135-154, https://doi.org/10.1016/0044-8486(92)90324-E.
Yao P, Lei L, Zhao B et al. 2019. Spatial-temporal variation of Aureococcus anophagefferens blooms in relation to environmental factors in the coastal waters of Qinhuangdao, China. Harmful Algae, 86: 106-118, https://doi.org/10.1016/j.hal.2019.05.011.
Zhang Q C, Qiu L M, Yu R C et al. 2012. Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China. Harmful Algae, 19: 117-124, https://doi.org/10.1016/j.hal.2012.06.007.
Zhang Q C, Yu R C, Zhao J Y et al. 2021. Distribution of Aureococcus anophagefferens in relation to environmental factors and implications for brown tide seed sources in Qinhuangdao coastal waters, China. Harmful Algae, 109:102105, https://doi.org/10.1016/j.hal.2021.102105.
Zhen Y, Qiao L, Gu B et al. 2016. Characteristics of eukaryotic microalgal community and its abiotic influencing factors during brown tide blooms near Qinhuangdao, China.Harmful Algae, 57: 1-12, https://doi.org/10.1016/j.hal.2016.05.001.
Zhukova N V. 2019. Fatty acids of marine mollusks: impact of diet, bacterial symbiosis and biosynthetic potential.Biomolecules, 9(12): 857, https://doi.org/10.3390/biom9120857.