Trophic upgrading of essential fatty acids by <i>Oxyrrhis marina</i>

Yu-ting WEI; Yan WANG; Xiao-dong WANG

doi:10.12111/j.mes20200301

Heterotrophic dinoflagellates serve as an intermediate bridge connecting zooplankton and phytoplankton, and play a key role in material recycling and energy flowing in marine ecosystems.In this paper, fatty acid of heterotrophic dinoflagellate Oxyrrhis marina was analyzed after feeding on four phytoplankton, including Dunaliella tertiolecta, Heterosigma akashiwo, Phaeocystis globosa, and Navicula salinarum.Research shows that O.marina can feed on four kinds of phytoplankton, but ingestion rate on D.tertiolecta was higher than those on other three species.DHA (docosahexaenoic acid) was not observed in all prey, but found in the O.marina fed on them with the content up to (86.98±7.44) μg/mg C.These results indicate that O.marina can synthesize DHA independently, which means that O.marina had the ability to upgrade the nutritional value of phytoplankton, thereby efficiently delivery docosahexaenoic acid to the next trophic level.

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异养甲藻(heterotrophic dinoflagellates)是一类以异养方式从外界获取物质和能量的原生生物，种类繁多，分布广泛^[1]。细胞表面存在鞭毛，依靠鞭毛的运动进行运动和摄食^[2]。海洋中异养甲藻摄食范围较为广泛^[3]，主要摄食海洋细菌和微型浮游植物，甚至能够摄食同自身粒径相近的食物。异养甲藻摄食对海洋细菌以及浮游植物的数量、结构和空间分布均有显著的影响。异养甲藻本身则被桡足类等中型浮游动物摄食，从而将物质和能量传递到更高营养级生物^[4-5]，成为连接微生物环和经典食物链的中枢环节。

长链ω3多不饱和脂肪酸(long-chain n-3 polyunsaturated fatty acids, LCn-3PUFA)，尤其是二十碳五烯酸(eicosapentaenoic acid, EPA; 20:5ω3)和二十二碳六烯酸(docosahexaenoic acid, DHA; 22:6ω3)是影响浮游动物生殖发育的重要因素^[6-9]。然而浮游动物自身无法合成这类必需脂肪酸，必须从食物中获取。由于很多浮游植物往往缺乏该类必需脂肪酸，当桡足类摄食这些浮游植物时则会导致其生殖效率下降。桡足类在摄食缺乏EPA和DHA的杜氏藻(Dunaliella tertiolecta)和球形棕囊藻(Phaeocystis globosa)后显示出较低的产卵率、卵孵化率和较高的幼体死亡率^[8-10]。但是在摄食异养甲藻后，桡足类的产卵率和卵的孵化率显著提高^{[9, 11]}，更多无节幼体发育为成体^[6]。这表明异养甲藻细胞可能含有浮游植物体内缺乏的必需脂肪酸，从而更好的支持了浮游动物的生殖发育。但是异养甲藻同样摄食浮游植物，也会面临食物中脂肪酸缺乏等问题，那么异养甲藻的必需脂肪酸从何而来？异养甲藻是否具有独立合成必需脂肪酸的能力？

本文选择海洋尖尾藻(Oxyrrhis marina)作为异养甲藻的代表，摄食不同种类浮游植物，研究海洋尖尾藻是否具有合成必需脂肪酸的功能。本研究有助于进一步了解异养甲藻对浮游动物种群结构和数量的影响。

3. 结论

海洋尖尾藻对杜氏藻、赤潮异弯藻、舟形藻和球形棕囊藻4种浮游植物均可摄食，粒径不同会导致摄食率不同。4种浮游植物均不含有DHA，海洋尖尾藻在摄食4种浮游植物后均检测出DHA，表明海洋尖尾藻具有独立合成DHA的能力。海洋尖尾藻这种独立合成脂肪酸的能力实现了对低质量食物的营养升级。

Reference (22)

[1]	LEE W J, PATTERSON D J. Diversity and geographic distribution of free-living heterotrophic flagellates-analysis by PRIMER[J]. Protist, 1998, 149(3): 229-244. doi: 10.1016/S1434-4610(98)70031-8
[2]	CORLISS J O, PATTERSON D J, LARSEN J. The biology of free-living heterotrophic flagellates[J]. Transactions of the American Microscopical Society, 1992, 111(3): 267-268. doi: 10.2307/3226616
[3]	WEISSE T, MÜLLER H. Planktonic protozoa and the microbial food web in Lake Constance[J]. Lake Constance:Characterization of an Ecosystem in Transition, 1998, 53(): 223-254.
[4]	GIEBELHAUSEN B, LAMPERT W. Temperature reaction norms of Daphnia magna:the effect of food concentration[J]. Freshwater Biology, 2001, 46(3): 281-289. doi: 10.1046/j.1365-2427.2001.00630.x
[5]	WEISSE T, STADLER P, LINDSTRÖM E S. Interactive effect of temperature and food concentration on growth rate:a test case using the small freshwater ciliate Urotricha farcta[J]. Limnology and Oceanography, 2002, 47(5): 1447-1455. doi: 10.4319/lo.2002.47.5.1447
[6]	BRETELER W C M K, SCHOGT N, BAAS M. Trophic upgrading of food quality by protozoans enhancing copepod growth:role of essential lipids[J]. Marine Biology, 1999, 135(1): 191-198. doi: 10.1007/s002270050616
[7]	MÜLLER-NAVARRA D C, BRETT M T, PARK S. Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes[J]. Nature, 2004, 427(6969): 69-72. doi: 10.1038/nature02210
[8]	KOSKI M, BRETELER W K, SCHOGT N. Effect of food quality on rate of growth and development of the pelagic copepodPseudocalanus elongatus (Copepoda, Calanoida)[J]. Marine Ecology Progress Series, 1998, 170(): 169-187. doi: 10.3354/meps170169
[9]	TANG K W, JAKOBSEN H H, VISSER A W. Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web:feeding, growth, and trophic interactions among grazers[J]. Limnology and Oceanography, 2001, 46(8): 1860-1870. doi: 10.4319/lo.2001.46.8.1860
[10]	LACOSTE A, POULET S A, CUEFF A. New evidence of the copepod maternal food effects on reproduction[J]. Journal of Experimental Marine Biology and Ecology, 2001, 259(1): 85-107. doi: 10.1016/S0022-0981(01)00224-6
[11]	BROGLIO E, JÓNASDÓTTIR S H, CALBET A. Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepodAcartia tonsa:relationship with prey fatty acid composition[J]. Aquatic Microbial Ecology, 2003, 31(3): 267-278.
[12]	GUILLARD R R L.Culture of phytoplankton for feeding marine invertebrates[M]//SMITH W L, CHANLEY M H.Culture of marine Invertebrate Animals.Boston, MA: Springer, 1975: 29-60.
[13]	O'HALLORAN C, SILVER M W, HOLMAN T R. Heterosigma akashiwo in central California waters[J]. Harmful Algae, 2006, 5(2): 124-132. doi: 10.1016/j.hal.2005.06.009
[14]	ROUSSEAU V, MATHOT S, LANCELOT C. Calculating carbon biomass of Phaeocystis sp.from microscopic observations[J]. Marine Biology, 1990, 107(2): 305-314. doi: 10.1007/BF01319830
[15]	ADMIRAAL W, BOUWMAN L A, HOEKSTRA L. Qualitative and quantitative interactions between microphytobenthos and herbivorous meiofauna on a brackish intertidal mudflat[J]. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 1983, 68(2): 175-191. doi: 10.1002/iroh.19830680203
[16]	DODGE J D, CRAWFORD R M. Fine structure of the dinoflagellateOxyrrhis marina II.The flagellar system[J]. Protistologica, 1971, 7(): 399-409.
[17]	FROST B W. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod calanus pacificus[J]. Limnology and Oceanography, 1972, 17(6): 805-815. doi: 10.4319/lo.1972.17.6.0805
[18]	FENCHEL T. Protozoan filter feeding[J]. Progress in Protistology, 1986, 1(): 65-113.
[19]	HANSEN P J. Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale[J]. Marine Biology, 1992, 114(2): 327-334. doi: 10.1007/BF00349535
[20]	TARRAN G A.Aspects of grazing behaviour of the marine dinoflagellateOxyrrhis marina, Dujardin[D].Soton: University of Southampton, 1991.
[21]	VELOZA A J, CHU F L E, TANG K W. Trophic modification of essential fatty acids by heterotrophic protists and its effects on the fatty acid composition of the copepodAcartia tonsa[J]. Marine Biology, 2006, 148(4): 779-788. doi: 10.1007/s00227-005-0123-1
[22]	SARGENT J R, WHITTLE K J.Lipids and hydrocarbons in the marine food web[M]//LONGHURST A R.Analysis of Marine Ecosystems.London: Academic Press, 1981: 491-533.

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Trophic upgrading of essential fatty acids by Oxyrrhis marina

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1.1. 材料

1.2. 实验方法

1.3. 统计分析方法

2.1. 结果

2.1.1. 海洋尖尾藻的摄食率

2.1.2. 浮游植物的脂肪酸

2.1.3. 海洋尖尾藻的脂肪酸

2.2. 讨论

Catalog

[1]	LEE W J, PATTERSON D J.Diversity and geographic distribution of free-living heterotrophic flagellates-analysis by PRIMER[J].Protist, 1998, 149(3):229-244. doi: 10.1016/S1434-4610(98)70031-8
[2]	CORLISS J O, PATTERSON D J, LARSEN J.The biology of free-living heterotrophic flagellates[J].Transactions of the American Microscopical Society, 1992, 111(3):267-268. doi: 10.2307/3226616
[3]	WEISSE T, MÜLLER H.Planktonic protozoa and the microbial food web in Lake Constance[J].Lake Constance:Characterization of an Ecosystem in Transition, 1998, 53:223-254.
[4]	GIEBELHAUSEN B, LAMPERT W.Temperature reaction norms of Daphnia magna:the effect of food concentration[J].Freshwater Biology, 2001, 46(3):281-289. doi: 10.1046/j.1365-2427.2001.00630.x
[5]	WEISSE T, STADLER P, LINDSTRÖM E S, et al.Interactive effect of temperature and food concentration on growth rate:a test case using the small freshwater ciliate Urotricha farcta[J].Limnology and Oceanography, 2002, 47(5):1447-1455. doi: 10.4319/lo.2002.47.5.1447
[6]	BRETELER W C M K, SCHOGT N, BAAS M, et al.Trophic upgrading of food quality by protozoans enhancing copepod growth:role of essential lipids[J].Marine Biology, 1999, 135(1):191-198. doi: 10.1007/s002270050616
[7]	MÜLLER-NAVARRA D C, BRETT M T, PARK S, et al.Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes[J].Nature, 2004, 427(6969):69-72. doi: 10.1038/nature02210
[8]	KOSKI M, BRETELER W K, SCHOGT N.Effect of food quality on rate of growth and development of the pelagic copepodPseudocalanus elongatus (Copepoda, Calanoida)[J].Marine Ecology Progress Series, 1998, 170:169-187. doi: 10.3354/meps170169
[9]	TANG K W, JAKOBSEN H H, VISSER A W.Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web:feeding, growth, and trophic interactions among grazers[J].Limnology and Oceanography, 2001, 46(8):1860-1870. doi: 10.4319/lo.2001.46.8.1860
[10]	LACOSTE A, POULET S A, CUEFF A, et al.New evidence of the copepod maternal food effects on reproduction[J].Journal of Experimental Marine Biology and Ecology, 2001, 259(1):85-107. doi: 10.1016/S0022-0981(01)00224-6
[11]	BROGLIO E, JÓNASDÓTTIR S H, CALBET A, et al.Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepodAcartia tonsa:relationship with prey fatty acid composition[J].Aquatic Microbial Ecology, 2003, 31(3):267-278.
[12]	GUILLARD R R L.Culture of phytoplankton for feeding marine invertebrates[M]//SMITH W L, CHANLEY M H.Culture of marine Invertebrate Animals.Boston, MA: Springer, 1975: 29-60.
[13]	O'HALLORAN C, SILVER M W, HOLMAN T R, et al.Heterosigma akashiwo in central California waters[J].Harmful Algae, 2006, 5(2):124-132. doi: 10.1016/j.hal.2005.06.009
[14]	ROUSSEAU V, MATHOT S, LANCELOT C.Calculating carbon biomass of Phaeocystis sp.from microscopic observations[J].Marine Biology, 1990, 107(2):305-314. doi: 10.1007/BF01319830
[15]	ADMIRAAL W, BOUWMAN L A, HOEKSTRA L, et al.Qualitative and quantitative interactions between microphytobenthos and herbivorous meiofauna on a brackish intertidal mudflat[J].Internationale Revue der gesamten Hydrobiologie und Hydrographie, 1983, 68(2):175-191. doi: 10.1002/iroh.19830680203
[16]	DODGE J D, CRAWFORD R M.Fine structure of the dinoflagellateOxyrrhis marina II.The flagellar system[J].Protistologica, 1971, 7:399-409.
[17]	FROST B W.Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod calanus pacificus[J].Limnology and Oceanography, 1972, 17(6):805-815. doi: 10.4319/lo.1972.17.6.0805
[18]	FENCHEL T.Protozoan filter feeding[J].Progress in Protistology, 1986, 1:65-113.
[19]	HANSEN P J.Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale[J].Marine Biology, 1992, 114(2):327-334. doi: 10.1007/BF00349535
[20]	TARRAN G A.Aspects of grazing behaviour of the marine dinoflagellateOxyrrhis marina, Dujardin[D].Soton: University of Southampton, 1991.
[21]	VELOZA A J, CHU F L E, TANG K W.Trophic modification of essential fatty acids by heterotrophic protists and its effects on the fatty acid composition of the copepodAcartia tonsa[J].Marine Biology, 2006, 148(4):779-788. doi: 10.1007/s00227-005-0123-1
[22]	SARGENT J R, WHITTLE K J.Lipids and hydrocarbons in the marine food web[M]//LONGHURST A R.Analysis of Marine Ecosystems.London: Academic Press, 1981: 491-533.