Academic Scientific JournalsIntercellular and extracellular amino acids of different bloom species in the Mediterranean Sea
DOI:
https://doi.org/10.26881/oandhs-2022.2.06Keywords:
Extracellular amino acids, Skeletonema costatum, Scrippsiella trochoidea, Ulva fasciata, Corallina officinalisAbstract
The presented laboratory experiment was designed to characterize the quantity and compositional variation of algal extracellular amino acids (AAs) that may represent an alternative nutrient source in a natural environment. To resemble algal bloom scenarios, analyses were conducted in mono- and/or co-cultures of the bloom-forming species Skeletonema costatum, Scrippsiella trochoidea, Ulva fasciata, and Corallina officinalis during their active growth phase. The study revealed that S. costatum exhibited higher production of the dominant AAs than S. trochoidea. Alanine, lysine, and threonine acids are the dominant amino acids in S. costatum and S. trochoidea filtrates, which may play a role in mucus formation during mucosal phytoplankton blooms with negative ecological effects. On the other hand, aspartic, glutamine, alanine, and leucine acids are the dominant amino acids in macroalgae. In co-culture experiments, U. fasciata shows strong and rapid allelopathic activity against these two potentially harmful species. The AA production offers an advantage to species with the capacity to absorb them to form blooms. Thus, anthropogenic inorganic nutrient inputs may be less important for the development of algal blooms in coastal waters. A major difference that distinguishes this work from others is the use of specific multi-taxa cultures of phytoplankton and macroalgae. The study represents a new research effort in Alexandria waters.
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Akgül, R., Bayram, K., Füsun, A., & Ormanc, H. B. (2015). Crude Protein Values and Amino Acid Profiles of Some Red Algae Collected from Çanakkale. International Journal of Molecular Sciences, 44(4), 527–530.
Aleem, A. A. (1993). The marine algae of Alexandria, Egypt, University Alexandria. pp 139. Anderson, D.M. & Cheng, T. P.-O. (1988). Intracellular localization of saxitoxins in the dinoflagellate Gonyaulax tamarensis. Journal of Phycology, 24, 17–22. https://doi. org/10.1111/j.1529-8817.1988.tb04451.x.
Bettarel, Y., Kan, J., Wang, K., Williamson, K. E., Cooney, S., Ribblett, S., Chen, F., Wommack, K. E., & Coats, D. W. (2005). Isolation and preliminary characterization of a small nuclear inclusion virus infecting the diatom Chaetoceros cf. gracilis. Aquatic Microbial Ecology, 40, 103–114. https://doi.org/10.3354/ame040103.
Bruckner, C.G., Rehm, C., Grossart, H.P. & Kroth, P.G. (2011). Growth and release of extracellular organic compounds by benthic diatoms depend on interactions with bacteria. Environmental Microbiology 13(4), 1052- 1063. https://doi.org/10.1111/j.1462-2920.2010.02411.x.
Bronk, D. A., & Glibert, P. M. (1993). Application of a 15 N tracer method to the study of dissolved organic nitrogen uptake during spring and summer in Chesapeake Bay. Marine Biology, 115(3), 501–508. https://doi.org/10.1007/ BF00349849.
Burpee, B., Saros, J. E., Northington, R. M., & Simon, K. S. (2016). Microbial nutrient limitation in Arctic lakes in a permafrost landscape of southwest Greenland. Biogeosciences, 13(2), 365–374. https://doi.org/10.5194/bg-13-365-2016.
Chen, T.-C., Ho, P.-C., Gong, G.-C., Tsai, A.-Y., & Hsieh C.-H. (2021). Finding Approaches to Exploring the Environmental Factors That Influence Copepod-Induced Trophic Cascades in the East China Sea. Diversity (Basel), 13(7), 299. https:// doi.org/10.3390/d13070299.
Derrien, A., Coiffard, L.J., Coiffard, C. & De RoeckHoltzhauer, Y. (1998). Free amino acid analysis of five microalgae. Journal of Applied Phycology 10(2), 131- 134. https://doi.org/10.1023/A:1008003016458.
Dixon, G. K., & Syrett, P. J. (1988). The growth of dinoflagellates in laboratory cultures. The New Phytologist, 109, 297– 302. https://doi.org/10.1111/j.1469-8137.1988.tb04198.x.
El-Sheekh, M. M., Khairy, H. M., & El-Shenody, R. A. (2010). Allelopathic effects of cyanobacterium Microcystis aeruginosa kützing on the growth and photosynthetic pigments of some algal species. Allelopathy Journal, 26(2), 75–290. https://doi.org/10.1007/s10457-010-9321-z.
El Shafay, S. M., Abo Shady, A. M., Abdel-Fatah, L. M., Hosny, Sh., & Labib, W. (2019). Allelopathic effect of the green macroalga Ulna fasciata (Delile) on species forming potentially harmful algal blooms. The Egyptian Journal of Experimental Biology (Botany), 15(2), 251–260. https://doi.org/10.5455/egyjebb.20190505044917.
Flynn, K. J., Clark, D. R., & Xue, Y. (2008). Modeling the release of dissolved organic matter by phytoplankton(1). Journal of Phycology, 44, 1171–1187. https://doi.org/10.1111/j.1529- 8817.2008.00562.x PMID:27041714.
Franklin, R.B. & Mills, A.L. (2006). Structural and functional responses of a sewage microbial community to dilutioninduced reductions in diversity. Microbial Ecology 52(2): 280-288. https://doi.org/10.1007/s00248-006-9033-0.
Glibert, P. M., Magnien, R., Lomas, M. W., Alexander, J., Fan, C., Haramoto, E., Trice, M. & Kana, T. M. (2001). Harmful algal blooms in the Chesapeake and coastal bays of Maryland, USA: Comparison of 1997, 1998, and 1999 events. Estuaries, 24(6), 875–883. https://doi.org/10.2307/1353178.
Granum, E., Kirkvold, S., & Myklestad, S. M. (2002). Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: Diel variations and effects of N depletion. Marine Ecology Progress Series, 242, 83–94. https://doi.org/10.3354/ meps242083.
Grosse, J., Burson, A., Stomp, M., Huisman, J. & Boschker, H.T. (2017). From ecological stoichiometry to biochemical composition: variation in N and P supply alters key biosynthetic rates in marine phytoplankton. Frontiers in Microbiology 8: 1299. https://doi.org/10.3389/fmicb.2017.01299.
Guillard, R. R. L. (1973). Division rates. In R. Stein (Ed.), Handbook of phycological methods: culture methods and growth measurements (pp. 290–311). Cambridge University Press.
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, 229–239. https://doi.org/10.1139/m62- 029 PMID:13902807.
Hallegraeff, G. M. (2002). Aquaculturists’ Guide to Harmful Australian Microalgae. School of Plant Science, 2nd ed. University of Tasmania, Hobart, Tasmania Australia. 136. ISBN 1-86295-049.
Henderson, J., Ricker, R., Bidlingmeyer, B., & Woodward, C. (2000). Rapid, accurate, sensitive and reproducible HPLC analysis of amino acids. In Application bulletin 5980– 1193. Agilent Technologies., https://www.agilent.com/cs/library/chromatograms/59801193.
Hounshell, A. G., Peierls, B. L., Osburn, C. L., & Paerl, H. W. (2017). Stimulation of phytoplankton production by anthropogenic dissolved organic nitrogen in a coastal plain estuary. Environmental Science & Technology, 51(22), 13104–13112. https://doi.org/10.1021/acs.est.7b03538 PMID:29083877.
Hosny, Sh. (2016). Ecological and Physiological Studies on the Interaction between Macroalgae and Phytoplankton off Alexandria Mediterranean Coast (Egypt). Thesis (Ph.D), Faculty of Science, Tanta University.
Horner, R. A., Postel, J. R., Halsband-Lenk, C., Pierson, J. J., Pohnert, G., & Wichard, T. (2005). Winter-spring phytoplankton blooms in Dabob Bay, Washington. Progress in Oceanography, 67, 286–313. https://doi.org/10.1016/j. pocean.2005.09.005.
Howard, A. G., Comber, S. D. W., Kifle, D., Antai, E. E., & Purdie, D. A. (1995). Arsenic speciation and seasonal changes in nutrient availability and micro-plankton abundance in Southampton Water, U. K. Estuarine, Coastal and Shelf Science, 40(4), 435–450. https://doi.org/10.1006/ecss.1995.0030.
Ibrahim, E. A., Zaher, S. S., Ibrahim, W. M., & Mosad, Y. A. (2021). Phytoplankton dynamics in relation to Red tide appearance in Qarun Lake, Egypt. Egyptian Journal of Aquatic Research, 47(3), 293–300. https://doi.org/10.1016/j. ejar.2021.07.005.
Ismail, G. A. (2017). Biochemical composition of some Egyptian seaweeds with potent nutritive and antioxidant properties. Food Science and Technology, 37, 294- 302. https://doi.org/10.1590/1678-457X.20316.
Kester, D., Duedall, I., Connors, D., & Pytkowicz, R. (1967). Preparation of artificial seawater. Limnology and Oceanography, 12, 176–179. https://doi.org/10.4319/ lo.1967.12.1.0176.
Kolmakova, A. A., & Kolmakov, V. I. (2019). Amino Acid Composition of Green Microalgae and Diatoms, Cyanobacteria, and Zooplankton [Review]. Inland Water Biology, 12(4), 452–461. https://doi.org/10.1134/ S1995082919040060.
Kujawinski, E. B. (2011). The impact of microbial metabolism on marine dissolved organic matter. Annual Review of Marine Science, 3, 567–599. https://doi.org/10.1146/ annurev-marine-120308-081003 PMID:21329217.
Labib, W. (2002). Phyto-zooplankton coupling off Alexandria (Egypt). Egyptian Journal of Aquatic Biology and Fisheries, 6(3), 59–84. https://doi.org/10.21608/ejabf.2002.1751.
El Shafay, S., Abo Shady, A., Abdel-Ftah, L. M., Ali, S. H., & Labib, W. (2019). Allelopathic effect of the green macroalgae Ulva fasciata (Delile) on potentially harmful algal bloom. The Egyptian Journal of Experimental Biology (Botany), 15(2), 169–180. https://doi.org/10.5455/ egyjebb.20190505044917.
Li, P., Mai, K., Trushenski, J., & Wu, G. (2009). New developments in fish amino acid nutrition: Towards functional and environmentally oriented aquafeeds. Amino Acids, 37(1), 43–53. https://doi.org/10.1007/s00726-008-0171- 1 PMID:18751871.
Li, H., Zhang, Y., Han, X., Shi, X., Rivkin, R. B., & Legendre, L. (2016). Growth responses of Ulva prolifera to inorganic and organic nutrients: Implications for macroalgal blooms in the southern Yellow Sea, China. Scientific Reports, 6, 26498. https://doi.org/10.1038/ srep26498 PMID:27199215.
Liu, Q., Tian, Y., Liu, Y., Yu, M., Hou, Z., He, K. & Jiang, Y. (2020). Relationship between dissolved organic matter and phytoplankton community dynamics in a humanimpacted subtropical river. Journal of Cleaner Production, 125-144. https://doi.org/10.1016/j.jclepro.2020.125144.
Lourenço, S. O., Barbarino, E., Lavín, P. L., Marquez, U. M. L., & Aidar, E. (2004). Distribution of intracellular nitrogen in marine microalgae. Calculation of new nitrogen-to-protein conversion factors. European Journal of Phycology, 39(1), 17–32. https://doi.org/10.1080/0967026032000157156.
Malone, T. C., & Newton, A. (2020). The globalization of cultural eutrophication in the coastal ocean: Causes and consequences. Frontiers in Marine Science, 7, 670. https:// doi.org/10.3389/fmars.2020.00670.
Mannino, A., & Harvey, H. R. (2000). Terrigenous dissolved organic matter along an estuarine gradient and its flux to the coastal ocean. Organic Geochemistry, 31(12), 1611– 1625. https://doi.org/10.1016/S0146-6380(00)00099-1.
Marsot, P., Cembella, A. D., & Colombo, J. C. (1991). Intracellular and extracellular amino acid pools of the marine diatom Phaeodactyllum tricornutum (bacillariophyceae) grown on unenriched seawater in high‐cell‐density dialysis culture. Journal of Phycology, 27(4), 478–491. https://doi. org/10.1111/j.0022-3646.1991.00478.x.
Martin-Jézéquel, V., Poulet, S. A., Harris, R. P., Moal, J., & Samain, J. F. (1988). Interspecific and intraspecific composition and variation of free amino acids in marine phytoplankton. Marine Ecology Progress Series, 44, 303– 313. https://doi.org/10.3354/meps044303.
Meksumpun, S., Montani, S., & Okaichi, T. (1994). Changes in Some Chemical Components of Alexandrium catenella and Scrippsiella trochoidea during Their Growth Cycles. Fisheries Science, 60(2), 207–212. https://doi. org/10.2331/fishsci.60.207.
Metaxatos, A., Panagiotopoulos, C. & Ignatiades, L. (2003). Monosaccharide and amino acid composition of mucilage material produced from a mixture of four phytoplanktonic taxa. Journal of Experimental Marine Biology and Ecology, 294(2), 203-217. https://doi.org/10.1016/S0022- 0981(03)00269-7.
Mikhail, S., Khalil, N., & El-Hadary, M. (2020). A new recorded of red tide forming species, Heterocapsa triquetra, Gymnodinium impudicum, Heterosigma akashiwo and Thalassiosira rotula in Alexandria Waters, Egypt. Egyptian Journal of Aquatic Biology and Fisheries, 24(6), 207–223. https://doi.org/10.21608/ejabf.2020.117258.
Mikhail, S., & Labib, W. (2014). Invasion-allelopathy interaction in the eutrophic coastal waters of Alexandria: Case of the invaders raphidophyte Chattonella antiqua and the dinoflagellates Alexandrium ostenfeldii and Gymnodinium catenatum. —International Congress On Estuaries & Coastal Protected Areas, ECPA 2014, 04 - 06 November 2014, Izmir – Turkey.
Miralto, A., Barone, G., Romano, G., Poulet, S. A., Ianora, A., Russo, G. L., Buttino, I., Mazzarella, G., Laabir, M., Cabrini, M., & Giacobbe, M. G. (1999). The insidious effect of diatoms on copepod reproduction. Nature, 402, 173–176. https:// doi.org/10.1038/46023.
Møller, E. F. (2007). Production of dissolved organic carbon by sloppy feeding in the copepods Acartia tonsa, Centropages typicus, and Temora longicornis. Limnology and Oceanography, 52, 79–84. https://doi.org/10.4319/ lo.2007.52.1.0079.
Moustafa, Y. T. A., & Eladel, H. M. H. M. (2015). Amino acids profile of Ulva sp. macroalgae collected from Alexandria coast in Egypt: A potential food resource Point Journal of Botany and Microbiology Research, 1(2): 015-022. https:// www.researchgate.net/publication/285235218.
Mulholland, M. R., Gobler, Ch. J., & Lee, C. (2002). Peptide hydrolysis, amino acid oxidation, and nitrogen uptake in communities seasonally dominated by Aureococcusanopha gefferens. Limnology and Oceanography, 47(4), 1094–1108. https://doi.org/10.4319/ lo.2002.47.4.1094.
Myklestad, S. (2000). Dissolved organic carbon from phytoplankton, p. 111–148. In: P. Wangersky [ed.]. The handbook of environmental chemistry. In Marine Chemistry. V. 5D. Springer.
Orellana, M. V., Pang, W. L., Durand, P. M., Whitehead, K. & Baliga, N. S. (2013). A role for programmed cell death in the microbial loop. Plos One. 8(5): e62595. https://doi. org/10.1371/journal.pone.0062595.
Sakamoto, S., Lim, W. A., Lu, D., Dai, X., Orlova, T., & Iwataki, M. (2021). Harmful algal blooms and associated fisheries damage in East Asia: Current status and trends in China, Japan, Korea and Russia. Harmful Algae,102, 101787. https://doi.org/10.1016/j.hal.2020.101787 PMID:33875176.
Sarmento, H., Romera-Castillo, C., Lindh, M., Pinhassi, J., Sala, M. M., Gasol, J., M., Marrase, C., & Taylor, G. T. (2013). Phytoplankton species-specific release of dissolved free amino acids and their selective consumption by bacteria. Limnology and Oceanography, 58(3), 1123– 1135. https://doi.org/10.4319/lo.2013.58.3.1123.
Sellner, K. G., & Nealley, E. W. (1997). Diel fluctuations in dissolved free amino acids and monosaccharides in Chesapeake Bay. Marine Chemistry, 56(3-4), 193– 200. https://doi.org/10.1016/S0304-4203(96)00069-2.
Suksomjit, M., Nagao, S., Ichimi, K., Yamada, T., & Tada, K. (2009). Variation of Dissolved Organic Matter and Fluorescence Characteristics before, during and after Phytoplankton bloom. Journal of Oceanography, 65, 835–846. https://doi. org/10.1007/s10872-009-0069-x.
Tang, Y. Z., & Gobler, C. J. (2012). The toxic dinoflagellate Cochlodinium polykrikoides (Dinophyceae) produces resting cysts. Harmful Algae, 20, 71–80. https:// doi.org/10.1016/j.hal.2012.08.001.
Tas, S., & Yilmaz, I. N. (2015). Potentially harmful microalgae and algal blooms in a eutrophic estuary in Turkey. Mediterranean Marine Science, 16, 432–443. https:// doi.org/10.12681/mms.1042.
Thornton, D. C. O. (2014). Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. European Journal of Phycology, 49(1), 20–46. https:// doi.org/10.1080/09670262.2013.875596.
Tyler, A. C., McGlathery, K. J., & Anderson, I. C. (2003). Benthic algae control sediment-water column fluxes of organic and inorganic nitrogen compounds in a temperate lagoon. Limnology and Oceanography, 48, 2125–2137. https://doi.org/10.4319/lo.2003.48.6.2125.
Tyler, A. C., McGlathery, K. J., & Macko, S. A. (2005). Uptake of urea and amino acids by the macroalgae Ulna lactuca (Chlorophyta) and Gracilaria vermiculophylla (Rhodophyta). Marine Ecology Progress Series, 294, 161–172. https://doi.org/10.3354/meps294161.
Utermöhl, H. (1958). Zur vervollkommnung der quantitativen phytoplankton-methodik: Mit 1 Tabelle und 15 abbildungen im Text und auf 1 Tafel. Internationale Vereinigung für theoretische und angewandte Limnologie: Mitteilungen, 9(1):1-38. https://doi.org/10.1080/05384680 .1958.11904091.
Vardi, A., Schatz, D., Beeri, K., Motro, U., Sukenik, A., Levine, A., & Kaplan, A. (2002). Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Current Biology, 12(20), 1767–1772. https://doi.org/10.1016/S0960-9822(02)01217-4 PMID:12401172.
Veldhuis, M. J. W., Kraay, G. W., & Timmermans, K. R. (2001). Cell death in phytoplankton: Correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. European Journal of Phycology, 36, 167–177. https://doi.org/10.1080/0967026 0110001735318.
Vidoudez, Ch., & Pohnert, G. (2012). Comparative metabolomics of the diatom Skeletonema marinoi in different growth phases. Metabolomics, 8, 654–669. https://doi. org/10.1007/s11306-011-0356-6.
Whitelegge, T. (1891). On the recent discoloration of the waters of Port Jackson. Records of the Australian Museum, 1, 179– 192. https://doi.org/10.3853/j.0067-1975.1.1891.1253.
Wu, G. (2009). Amino acids: Metabolism, functions, and nutrition. Amino Acids,37(1), 1–17. https://doi.org/10.1007/ s00726-009-0269-0 PMID:19301095.
Xiao, J., Zhang, X., Gao, C., Jiang, M., Li, R., Wang, Z., Li, Y., Fan, S., & Zhang, X. (2016). Effect of temperature, salinity and irradiance on growth and photosynthesis of Ulva prolifera. Acta Oceanologica Sinica, 35(10), 114– 121. https://doi.org/10.1007/s13131-016-0891-0.
Yamamoto, T., Oh, S. J. & Kataoka, Y. (2004). Growth and uptake kinetics for nitrate, ammonium and phosphate by the toxic dinoflagellate Gymnodinium catenatum isolated from Hiroshima Bay. Japan Fisheries Science, 70 (1): 108- 115. https://doi.org/10.1111/j.1444-2906.2003.00778.x.
Zingone, A. Tim & Wyatt. (2012). Harmful algal blooms: keys to the understanding of phytoplankton ecology. The Sea. Harvard University Press, Harvard. 13: 867-926. https:// www.researchgate.net/publication/284429375.
Zhang, J., Xiao, T., Huang, D., Liu, S. M., & Fang, J. (2016). Editorial: Eutrophication and hypoxia and theirimpacts on the ecosystem of the Changjiang Estuary and adjacent coastal environment. Journal of Marine Systems, 154, 1–4. https://doi.org/10.1016/j. jmarsys.2015.10.007.
