The Effect of UV Light and CO₂ in the Production of Polyunsaturated Aldehydes in Skeletonema costatum (Bacillariophycea)

Luiz Felipe C. da Motta Pacheco¹, Eduardo Uribe¹, Jorge Pino², José Troncoso², Andrés Quiróz³

¹Laboratório de Producción Primaria, Facultad de Cienciasdel Mar, Universidad Católica del Norte, Coquimbo, Chile.
²EWOS Innovation, Bergen, Norway.
³Laboratório de Química Ecológica, Instituto de Química, Universidad de La Frontera, Temuco, Chile.

DOI: 10.4236/ajps.2014.524379                

Abstract

Skeletonema costatum was submitted to two experiments using UV lights and CO2with the purpose of observing changes in the lipids profile and the synthesis of polyunsaturated aldehydes (PUA) after cell disruption. When cells receive CO2 supply, it was noticed that the production of PUA was significantly lower. The same was observed when the culture was treated with a dose of 45.9 kJ·m^-2 of ultra-violet A/B ray. The premise to all experiments was the production of 2,4-heptadienal compared to the supply of EPA as substrate. As a result, the same synthesis rate was observed both when the CO2 treatment was applied and in the experiment control. On the other hand, the culture subjected to ultraviolet radiation showed a 68% greater demand with the utilization of the substrate. These observations suggested that EPA was consumed before cell disruption and was probably exuded to the surrounding environment as a sign of stress. Changes in cell morphology could be observed by the migration of the chloroplast nearby the cell wall, where PUA was produced, indicating a defense strategy.

Keywords

Diatom, Physiology, Oxilipins, Skeletonema costatum, Polyunsaturated Aldehyde (PUA)

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Allen, A.E., Vardi, A. and Bowler, C. (2006) An Ecological and Evolutionary Context for Integrated Nitrogen Metabolism and Related Signaling Pathways in Marine Diatoms. Current Opinion in Plant Biology, 9, 264-273. http://dx.doi.org/10.1016/j.pbi.2006.03.013
[2]	Nelson, D.M., Tréguer, P., Brzezinski, M.A., Leynaert, A. and Quéguiner, B. (1995) Production and Dissolution of Biogenic Silica in the Ocean: Revisid Global Estimates, Comparison with Regional Data and Relationship to Biogenic Sedimentation. Global Biogeochemical Cycle, 9, 359-372. http://dx.doi.org/10.1029/95GB01070
[3]	Yoshinga, M.Y., Sumida, P.Y.G., Silveria, I.C.A., Ciotti, A.M., Gaeta, S.A., Pacheco, L.F.M. and Koettker, A.G. (2010) Vertical Distribution of Benthic Invertebrate Larvae during an Upwelling Event along a Transect off the Tropical Brazilian Continental Margin. Journal of Marine Systems, 79, 124-133. http://dx.doi.org/10.1016/j.jmarsys.2009.07.007
[4]	Ribalet, F., Wichard, T., Pohnert, G., Ianora, A., Milarto A. and Casotti, R. (2007) Age and Nutrient Limitation Enhance Polyunsaturated Aldehyde Production in Marine Diatoms. Phytochemistry, 68, 2059-2067. http://dx.doi.org/10.1016/j.phytochem.2007.05.012
[5]	Ribalet, F., Vidoudez, C., Cassin, D., Pohnert, G., Ianora, A., Miralto, A. and Casotti. R. (2009) High Plasticity in the Production of Diatom-Derived Polyunsaturated Aldehydes under Nutrient Limitation: Physiological and Ecological Implications. Protist, 160, 444-451. http://dx.doi.org/10.1016/j.protis.2009.01.003
[6]	Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R.M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R.G., Plattner, G.K., Rodgers, K.B., Sabine, C.L. Sarmiento, J.L., Schlitzer, R., Slater, R.D., Totterdell, I.J., Weirig, M.F., Yamanaka, Y. and Yool, A. (2005) Anthropogenic Ocean Acidification over the Twenty-First Century and Its Impact on Calcifying Organisms. Nature, 437, 681-686. http://dx.doi.org/10.1038/nature04095
[7]	Doney, S.C., Fabry, V.J., Feely, R.A. and Kleypas, J.A. (2009) Ocean Acidification: The Other CO2 Problem. Annual Review of Marine Science, 1, 169-192. http://dx.doi.org/10.1146/annurev.marine.010908.163834
[8]	Engelsen, O. and Kylling, A. (2005) Fast Simulation Tool for Ultraviolet Radiation at the Earth’s Surface. Optical Engineering, 4, 44. http://nadir.nilu.no/~olaeng/fastrt/fastrt.html http://dx.doi.org/10.1117/1.1885472
[9]	Reuder, J., Dameris, M. and Koepke, P. (2001) Future UV Radiation in Central Europe Modelled from Ozone Scenarios. Journal of Phytochemistry and Photobiology B: Biology, 61, 94-105.
[10]	Riebesell, U., Schulz, K.G., Bellerby, R.G.J., Botros, M., Fritsche, P., Meyerhöfer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J. and Zöllner, E. (2007) Enhanced Biological Carbon Consumption in a High CO2 Ocean. Nature, 450, 545-548. http://dx.doi.org/10.1038/nature06267
[11]	Fontugne, M.R. and Descolas-Gros, C. (1985) Carbon Fixation in Marine Phytoplankton: Carboxylase Activities and Stable Carbon-Isotope Ratios; Physiological and Paleoclimatological Aspects. Marine Biology, 87, 1-6. http://dx.doi.org/10.1007/BF00396999
[12]	Wichard, T., Poulet, S.A., Halsband-Lenk, C., Albaina, A., Harris, R., Liu, D.Y. and Pohnert, G. (2005) Survey of the Chemical Defence Potential of Diatoms: Screening of Fifty One Species for Alpha, Beta, Gamma, Delta-Unsaturated Aldehydes. Journal of Chemical Ecology, 31, 949-958. http://dx.doi.org/10.1007/s10886-005-3615-z
[13]	Caldwell, G.S., Bentley, M.G. and Olive, P.J.W. (2003) The Use of a Brine Shrimp (Artemia salina) Bioassay to Assess the Toxicity of Diatom Extracts and Short Chain Aldehydes. Toxicon, 42, 301-306. http://dx.doi.org/10.1016/S0041-0101(03)00147-8
[14]	Romano, G., Russo, G.L., Buttino, I., Ianora, A. and Miralto, A. (2003) A Marine Diatom-Derived Aldehyde Induces Apoptosis in Copepod and Sea Urchin Embryos. Journal of Experimental Biology, 206, 3487-3494. http://dx.doi.org/10.1242/jeb.00580
[15]	Buttino, I., Santo, M.D., Ianora, A. and Miralto, A. (2004) Rapid Assessment of Copepod (Calanus helgolandicus) Embryo Viability Using Fluorescent Probes. Marine Biology, 145, 393-399. http://dx.doi.org/10.1007/s00227-004-1317-7
[16]	Ianora, A., Miralto, A., Poulet, S.A., Carotenuto, Y., Buttino, I., Romano, G., Casotti, R., Pohnert, G., Wichard, T., Colucci-D’Amato, L., et al. (2004) Aldehyde Suppression of Copepod Recruitment in Blooms of a Ubiquitous Planktonic Diatom. Nature, 429, 403-407. http://dx.doi.org/10.1038/nature02526
[17]	Miralto, A., Barone, G., Romano, G., Poulet, S.A., Ianora, A., Russo, G.L., Buttino, I., Mazzarella, G., Laabir, M., Cabrini, M., et al. (1999) The Insidious Effect of Diatoms on Copepod Reproduction. Nature, 402, 173-176. http://dx.doi.org/10.1038/46023
[18]	Vidoudez, C. and Pohnert, G. (2008) Growth Phase-Specific Release of Polyunsaturated Aldehydes by the Diatom Skeletonema marinoi. Journal of Plankton Research, 30, 1305-1313. http://dx.doi.org/10.1093/plankt/fbn085
[19]	Casotti, R., Mazza, S., Brunet, C., Vantrepotte, V., Ianora, A. and Miralto, A. (2005) Growth Inhibition and Toxicity of the Diatom Aldehyde 2-Trans, 4-Trans-Decadienal on Thalassiosira weissflogii (Bacillariophyceae). Journal of Phycology, 41, 7-20. http://dx.doi.org/10.1111/j.1529-8817.2005.04052.x
[20]	Ribalet, F., Berges, J.A., Ianora, A. and Casotti, R. (2007) Growth Inhibition of Cultured Marine Phytoplankton by Toxic Algal-Derived Polyunsaturated Aldehydes. Aquatic Toxicology, 85, 219-227. http://dx.doi.org/10.1016/j.aquatox.2007.09.006
[21]	Caldwell, G.S. (2009) Review-The Influence of Bioactive Oxylipins from Marine Diatoms on Invertebrate Reproduction and Development. Marine Drugs, 7, 367-400. http://dx.doi.org/10.3390/md7030367
[22]	Gallina, A.A., Brunet, C., Palumbo, A. and Casotti, R. (2014) The Effect of Polyunsaturated Aldehydes on Skeletonema marinoi (Bacillariophyceae): The Involvement of Reactive Oxygen Species and Nitric Oxide. Marine Drugs, 12, 4165-4187. http://dx.doi.org/10.3390/md12074165
[23]	Vardi, A. (2008) Cell Signaling in Marine Diatoms. Communicative & Integrative Biology, 1, 134-136. http://dx.doi.org/10.4161/cib.1.2.6867
[24]	Pohnert, G. (2000) Wound-Activated Chemical Defense in Unicellular Planktonic Algae. Angewandte Chemie International Edition, 30, 4352-4354. http://dx.doi.org/10.1002/1521-3773(20001201)39:23<4352::AID-ANIE4352>3.0.CO;2-U
[25]	Guillard, R.R.L. (1975) Culture of Phytoplankton for Feeding Marine Invertebrates. In: Smith, W.L. and Chanley, M.H., Eds., Culture of Marine Invertebrate Animals, Plenum Press, New York, 29-60.
[26]	Dring, M.J. (1982) The Biology of Marine Plants. Cambridge University Press, New York.
[27]	Kouwenberg, J.H.M. and Lantonie, F. (2007) Effects of Ultraviolet-B Stressed Diatom Food on the Reproductive Output in Mediterranean Calanus helgolandiscus (Crustacea; Copepoda). Journal of Experimental Marine Biology and Ecology, 341, 239-253. http://dx.doi.org/10.1016/j.jembe.2006.10.047
[28]	Lewis, T., Nichols, P.D. and McMeekin, T.A. (2000) Evaluation of Extraction Methods for Recovery of Fatty Acids from Lipid-Producing Microheterotrophs. Journal of Microbiological Methods, 43, 107-116. http://dx.doi.org/10.1016/S0167-7012(00)00217-7
[29]	Wichard, T., Poulet, S.A. and Pohnert, G. (2005) Determination and Quantification of α, β, γ, δ-Unsaturated Aldehydes as Pentaflurobenzyl-Oxime Derivatives in Diatom Cultures and Natural Phytoplankton Populations: Application in Marine Field Studies. Journal of Chromatography B, 814, 155-161. http://dx.doi.org/10.1016/j.jchromb.2004.10.021
[30]	Blanchemain, A. and Grizean, D. (1999) Increased Production of Eicosapentaenoic Acid by Skeletonema costatum Cells after Decantation at Low Temperature. Biotechnology Techniques, 13, 497-501. http://dx.doi.org/10.1023/A:1008989730798
[31]	Chen, X.W. and Gao, K.S. (2004) Characterization of Diurnal Photosynthetic Rhythms in the Marine Diatom Skeletonema costatum Grown in Synchronous Culture under Ambient and Elevated CO2. Functional Plant Biology, 31, 399-404. http://dx.doi.org/10.1071/FP03240
[32]	Armbrust, E.V., Berges, J.A., Bowler, C., Green, B.R., Martinez, D., Putnam, N.H., et al. (2004) The Genome of the Diatom Thalassiosira pseudonana: Ecology, Evolution, and Metabolism. Science, 306, 79-86. http://dx.doi.org/10.1126/science.1101156
[33]	Monsalve, J.R.B. (2010) Effect of CO2 on Elemental Composition and Fatty Acids of Diatoms and Concomitant Effects on Copepods. Master Thesis, Kiel University, Kiel.
[34]	Gieskes, W.W.C. and Buma, A.G.J. (1997) UV Damage to Plant Life in a Photobiologically Dynamic Environment: the Case of Marine Phytoplankton. Plant Ecology, 128, 17-25 (in Kouwenberg et al. 2007).
[35]	Neale, P.J., Davis, R.F. and Cullen, J.J. (1998) Interactive Effects of Ozone Depletion and Vertical Mixing on Photosynthesis of Antartic Phytoplankton. Nature, 392, 585-589 (in Kouwenberg et al. 2007).
[36]	Browlee, C. (2008) Diatom Signalling: Deadly Messages. Current Biology, 18, 518-519. http://dx.doi.org/10.1016/j.cub.2008.05.003
[37]	Ianora, A., Boersma, M., Casotti, R., Fontana, A., Harder, J., Hoffmann, F., et al. (2006) The H.T. Odum Synthesis Essay: New Trends in Marine Chemical Ecology. Estuaries and Coasts, 29, 531-551. http://dx.doi.org/10.1007/BF02784281
[38]	Vidoudez, C. and Pohnert, G. (2008) Growth Phase-Specific Release of Polyunsaturated Aldehydes by the Diatom Skeletonema marinoi. Journal of Plankton Research, 30, 1305-1313. http://dx.doi.org/10.1093/plankt/fbn085
[39]	Vidoudez, C., Nejstgaard, J.C., Jakobsen, H.H. and Pohnert, G. (2011) Dynamics of Dissolved and Particulate Polyunsaturated Aldehydes in Mesocosms Inoculated with Different Densities of the Diatom Skeletonema marinoi. Marine Drugs, 9, 345-358. http://dx.doi.org/10.3390/md9030345
[40]	Wichard, T., Gerecht, A., Boersma, M., Poulet, S.A., Wiltshire, K. and Pohnert, G. (2007) Lipid and Fatty Acid Composition of Diatoms Revisited: Rapid Wound-Activated Change of Food Quality Parameters Influences Herbivorous Copepod Reproductive. ChemBioChem, 8, 1146-1153. http://dx.doi.org/10.1002/cbic.200700053