|
|
Cite this paper: |
|
|
SHANG Lixia, HU Zhangxi, TANG Yingzhong. Identification of dissolved and particulate carbonyl compounds produced by marine harmful algal bloom species[J]. Journal of Oceanology and Limnology, 2019, 37(5): 1566-1581 |
|
|
|
|
|
|
|
Identification of dissolved and particulate carbonyl compounds produced by marine harmful algal bloom species |
|
| SHANG Lixia1,2,3, HU Zhangxi1,2,3, TANG Yingzhong1,2,3 |
|
1 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China;
3 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China |
|
| Abstract: |
| Carbonyl compounds, especially polyunsaturated aldehydes (PUAs), are increasingly reported as teratogenic to grazers and deleterious to phytoplankton. While PUAs have been considered to be mainly produced by diatoms after cell wounding, little is known about whether microalgae other than diatoms, particularly harmful algal bloom (HAB)-forming species, produce carbonyl compounds. In this study, we analyzed the carbonyl compounds from eight common HAB-forming species (Akashiwo sanguinea, Karenia mikimotoi, Karlodinium veneficum, Margalefidinium polykrikoides, Prorocentrum donghaiense, P. minimum, Scrippsiella trochoidea, and Heterosigma akashiwo) using gas chromatography-mass spectrometry in full scan and selected ion monitoring (SIM) modes. Our results show a ubiquitous presence of carbonyl compounds in both dissolved and particulate forms in all species we examined. In the full scan mode, 133 chromatographic peaks were detected from 51 samples altogether. Both the varieties of carbonyl compounds and their quantities were algal species dependent, although most of the carbonyl compounds could not be fully identified according to the mass spectral database only due to the unavailability of enough standards for all analytes. Aided with nine standards in SIM mode, we further identified and quantified all nine aldehydes (2-methyl-2-pentenal, trans-2-nonenal, cis-6-nonenal, 2,6-dimethyl-5-heptenal, trans-2-hexenal, trans-2-decenal, 2,4-heptadienal, trans-trans-2,4-octadienal, and trans-trans-2,4-decadienal). Four of these nine aldehydes were detected in particulate form, which confirmed that trans-2-nonenal could be produced by K. mikimotoi, Karl. veneficum, P. donghaiense, P. minimum, S. trochoidea, and H. akashiwo, 2,4-heptadienal and trans-trans-2,4-decadienal by A. sanguinea, M. polykrikoides, and S. trochoidea, and trans, trans-2,4-octadienal by S. trochoidea, respectively. We proved that some dinoflagellate and raphidophyte species could contribute to the pool of carbonyl compounds including PUAs in a marine ecosystem. Some carbonyl compounds, particularly those in high cell quota and/or dissolved concentration, may be related to fishkilling or allelopathy which needs further identification and quantification. |
|
| Key words:
aldehyde|dinoflagellate|harmful algal blooms (HABs)|heptadienal|octadienal|decadienal
|
|
| Received: 2018-08-23 Revised: 2018-11-21 |
|
|
|
|
References:
Anderson D M, Cembella A D, Hallegraeff G M. 2012.Progress in understanding harmful algal blooms:paradigm shifts and new technologies for research, monitoring, and management. Annual Review of Marine Science, 4:143-176.
Aráoz R, Molgó J, de Marsac N T. 2010. Neurotoxic cyanobacterial toxins. Toxicon, 56(5):813-828.
Bachvaroff T R, Adolf J E, Squier A H, Harvey H R, Place A R. 2008. Characterization and quantification of karlotoxins by liquid chromatography-mass spectrometry. Harmful Algae, 7(4):473-484.
Bao M L, Pantani F, Griffini O, Burrini D, Santianni D, Barbieri K. 1998. Determination of carbonyl compounds in water by derivatization-solid-phase microextraction and gas chromatographic analysis. Journal of Chromatography A, 809(1-2):75-87.
Barofsky A, Pohnert G. 2007. Biosynthesis of polyunsaturated short chain aldehydes in the diatom Thalassiosira rotula.Organic Letters, 9(6):1 017-1 020.
Bartual A, Arandia-Gorostidi N, Cózar A, Morillo-García S, Jesus Ortega M, Vidal M, Cabello A M, GonzálezGordillo J I, Echevarría F. 2014. Polyunsaturated aldehydes from large phytoplankton of the Atlantic Ocean surface (42°N to 33°S). Marine Drugs, 12(2):682-699.
Blossom H E, Rasmussen S A, Andersen N G, Larsen T O, Nielsen K F, Hansen P J. 2014. Prymnesium parvum revisited:relationship between allelopathy, ichthyotoxicity, and chemical profiles in 5 strains. Aquatic Toxicology, 157:159-166.
Cai P J, He S, Zhou C X, Place A R, Haq S, Ding L J, Chen H M, Jiang Y, Guo C, Xu Y R, Zhang J R, Yan X J. 2016.Two new karlotoxins found in Karlodinium veneficum(strain GM2) from the East China Sea. Harmful Algae, 58:66-73.
Carotenuto Y, Wichard T, Pohnert G, Lampert W. 2005. Lifehistory responses of Daphnia pulicaria to diets containing freshwater diatoms:effects of nutritional quality versus polyunsaturated aldehydes. Limnology and Oceanography, 50(2):449-454.
Castellano I, Ercolesi E, Romano G, Ianora A, Palumbo A. 2015. The diatom-derived aldehyde decadienal affects life cycle transition in the ascidian Ciona intestinalis through nitric oxide/ERK signalling. Open Biology, 5(3):140 182.
Cusick K D, Sayler G S. 2013. An overview on the marine neurotoxin, saxitoxin:genetics, molecular targets, methods of detection and ecological functions. Marine Drugs, 11(4):991-1 018.
da Silva V M, da Cunha Veloso M C, Teixeira Sousa E, Santos G V, Accioly MC, de P Pereira P A, de Andrade J B. 2006.Determination of 11 low-molecular-weight carbonyl compounds in marine algae by high-performance liquid chromatography. Journal of Chromatographic Science, 44(5):233-238.
d'Ippolito G, Tucci S, Cutignano A, Romano G, Cimino G, Miralto A, Fontana A. 2004. The role of complex lipids in the synthesis of bioactive aldehydes of the marine diatom Skeletonema costatum. Biochimica et Biophysica ActaMolecular and Cell Biology of Lipids, 1686(1-2):100-107.
Dittami S M, Wichard T, Malzahn A M, Pohnert G, Boersma M, Wiltshire K H. 2010. Culture conditions affect fatty acid content along with wound-activated production of polyunsaturated aldehydes in Thalassiosira rotula(Coscinodiscophyceae). In:Proceedings of the 7th International Chrysophyte Symposium. Nova Hedwigia, New London. p.231-248.
Dorantes-Aranda J J, Seger A, Mardones J I, Nichols P D, Hallegraeff G M. 2015. Progress in understanding algal bloom-mediated fish kills:the role of superoxide radicals, phycotoxins and fatty acids. PLoS One, 10(7):e0133549.
Edelkraut F, Brockmann U. 1990. Simulataneous determination of carboxylic acids and carbonyl compounds in estuaries by HPLC. Chromatographia, 30(7-8):432-435.
Fux E, Smith J L, Tong M M, Guzmán L, Anderson D M. 2011.Toxin profiles of five geographical isolates of Dinophysis spp. from North and South America. Toxicon, 57(2):275-287.
Gardner H W, Dornbos Jr D L, Desjardins A E. 1990. Hexanal, trans-2-hexenal, and trans-2-nonenal inhibit soybean, Glycine max, seed germination. Journal of Agricultural and Food Chemistry, 38(6):1 316-1 320.
Gayoso A M, Dover S L, Morton S L, Busman M, Moeller P D R, Fulco V K, Maranda L. 2002. Diarrhetic shellfish poisoning associated with Prorocentrum lima(Dinophyceae) in Patagonian Gulfs (Argentina). Journal of Shellfish Research, 21(2):461-463.
Grimshaw J. 1991. Hydroxy-aldehydes and -ketones and related compounds:dicarbonyl compounds. In:Sainsbury M ed. Second Supplements to the 2nd Edition of Rodd's Chemistry of Carbon Compounds. Elsevier, Amsterdam.p.53-107.
Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In:Smith W L, Chanley M H eds.Culture of Marine Invertebrate Animals. Plenum Press, New York. p.26-60.
Hallegraeff G M, Blackburn S I, Doblin M A, Bolch C J S. 2012. Global toxicology, ecophysiology and population relationships of the chainforming PST dinoflagellate Gymnodinium catenatum. Harmful Algae, 14:130-143.
Hansen E, Ernstsen A, Eilertsen H C. 2004. Isolation and characterisation of a cytotoxic polyunsaturated aldehyde from the marine phytoplankter Phaeocystis pouchetii(Hariot) Lagerheim. Toxicology, 199(2-3):207-217.
Heil C A, Glibert P M, Fan C L. 2005. Prorocentrum minimum(Pavillard) Schiller:a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae, 4(3):449-470.
Hillebrand H, Dürselen C D, Kirschtel D, Pollingher U, Zohary T. 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 35(2):403-424.
Holland P T, Selwood A I, Mountfort D O, Wilkins A L, McNabb P, Rhodes L L, Doucette G J, Mikulski C M, King K L. 2005. Isodomoic acid C, an unusual amnesic shellfish poisoning toxin from Pseudo-nitzschia australis.Chemical Research in Toxicology, 18(5):814-816.
Ianora A, Miralto A. 2010. Toxigenic effects of diatoms on grazers, phytoplankton and other microbes:a review.Ecotoxicology, 19(3):493-511.
Ianora A, Poulet S A, Miralto A. 1995. A comparative study of the inhibitory effect of diatoms on the reproductive biology of the copepod Temora stylifera. Marine Biology, 121(3):533-539.
Ianora A, Poulet S A. 1993. Egg viability in the copepod Temora stylifera. Limnology and Oceanography, 38(8):1 615-1 626.
Kieber R J, Zhou X L, Mopper K. 1990. Formation of carbonyl compounds from UV-induced photodegradation of humic substances in natural waters:fate of riverine carbon in the sea. Limnology and Oceanography, 35(7):1 503-1 515.
Kim D, Yamasaki Y, Yamatogi T, Yamaguchi K, Matsuyama Y, Kang Y S, Lee Y, Oda T. 2009. The possibility of reactive oxygen species (ROS)-independent toxic effects of Cochlodinium polykrikoides on damselfish (Chromis caerulea). Bioscience, Biotechnology, and Biochemistry, 73(3):613-618.
Kozakai H, Oshima Y, Yasumoto T. 1982. Isolation and structural elucidation of hemolysin from the phytoflagellate Prymnesium parvum. Agricultural and Biological Chemistry, 46(1):233-236.
Landsberg J H. 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, 10(2):113-390.
Le Lacheur R M, Sonnenberg L B, Singer P C, Christman R F, Charles M J. 1993. Identification of carbonyl compounds in environmental samples. Environmental Science & Technology, 27(13):2 745-2 753.
Leflaive J, Ten-Hage L. 2009. Chemical interactions in diatoms:role of polyunsaturated aldehydes and precursors.New Phytologist, 184(4):794-805.
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(6758):173-176.
Mooney B D, Hallegraeff G M, Place A R. 2010. Ichthyotoxicity of four species of gymnodinioid dinoflagellates(Kareniaceae, Dinophyta) and purified karlotoxins to larval sheepshead minnow. Harmful Algae, 9(6):557-562.
Mooney B D, Nichols P D, de Salas M F, Hallegraeff G M. 2007. Lipid, fatty acid, and sterol composition of eight species of Kareniaceae (Dinophyta):chemotaxonomy and putative lipid phycotoxins. Journal of Phycology, 43(1):101-111.
Nemecek-Marshall M, Wojciechowski C, Kuzma J, Silver G M, Fall R. 1995. Marine vibrio species produce the volatile organic compound acetone. Applied and Environmental Microbiology, 61(1):44-47.
Okolodkov Y B. 2005. The global distributional patterns of toxic, bloom dinoflagellates recorded from the Eurasian Arctic. Harmful Algae, 4(2):351-369.
Orlova T Y, Selina M S, Lilly E L, Kulis D M, Anderson D M. 2007. Morphogenetic and toxin composition variability of Alexandrium tamarense (Dinophyceae) from the east coast of Russia. Phycologia, 46(5):534-548.
Otero A, Chapela M J, Atanassova M, Vieites J M, Cabado A G. 2011. Cyclic imines:chemistry and mechanism of action:a review. Chemical Research in Toxicology, 24(11):1 817-1 829.
Pistocchi R, Guerrini F, Pezzolesi L, Riccardi M, Vanucci S, Ciminiello P, Dell'Aversano C, Forino M, Fattorusso E, Tartaglione L, Milandri A, Pompei M, Cangini M, Pigozzi S, Riccardi E. 2012. Toxin levels and profiles in microalgae from the North-Western Adriatic Sea-15 years of studies on cultured species. Marine Drugs, 10(1):140-162.
Pohnert G, Lumineau O, Cueff A, Adolph S, Cordevant C, Lange M, Poulet S A. 2002. Are volatile unsaturated aldehydes from diatoms the main line of chemical defence against copepods? Marine Ecology Progress Series, 245:33-45.
Pohnert G. 2000. Wound-activated chemical defense in unicellular planktonic algae. Angewandte Chemie International Edition, 39(23):4 352-4 354.
Rasmussen S A, Andersen A J C, Andersen N G, Nielsen K F, Hansen P J, Larsen T O. 2016. Chemical diversity, origin, and analysis of phycotoxins. Journal of Natural Products, 79(3):662-673.
Ribalet F, Vidoudez C, Cassin D, Pohnert G, Ianora A, Miralto A, Casotti R. 2009. High plasticity in the production of diatom-derived polyunsaturated aldehydes under nutrient limitation:physiological and ecological implications.Protist, 160(3):444-451.
Ribalet F, Wichard T, Pohnert G, Ianora A, Miralto A, Casotti R. 2007. Age and nutrient limitation enhance polyunsaturated aldehyde production in marine diatoms.Phytochemistry, 68(15):2 059-2 067.
Romero M L J, Kotaki Y, Lundholm N, Thoha H, Ogawa H, Relox J R, Terada R, Takeda S, Takata Y, Haraguchi K, Endo T, Lim P T, Kodama M, Fukuyo Y. 2011. Unique amnesic shellfish toxin composition found in the South East Asian diatom Nitzschia navis-varingica. Harmful Algae, 10(5):456-462.
Sansone C, Braca A, Ercolesi E, Romano G, Palumbo A, Casotti R, Francone M, Ianora A. 2014. Diatom-derived polyunsaturated aldehydes activate cell death in human cancer cell lines but not normal cells. PLoS One, 9(7):e10122.
Sasaki M, Takeda N, Fuwa H, Watanabe R, Satake M, Oshima Y. 2006. Synthesis of the JK/LM-ring model of prymnesins, potent hemolytic and ichthyotoxic polycyclic ethers isolated from the red tide alga Prymnesium parvum:confirmation of the relative configuration of the K/L-ring juncture. Tetrahedron Letters, 47(32):5 687-5 691.
Shahraki J, Motallebi A, Aghvami M, Pourahmad J. 2013.Ichthyotoxic Cochlodinium polykrikoides induces mitochondrial mediated oxidative stress and apoptosis in rat liver hepatocytes. Iranian Journal of Pharmaceutical Research, 12(4):829-844.
Sun K, Qiu Z F, He Y J, Fan W, Wei Z X. 2017. Vertical development of a Prorocentrum donghaiense bloom in the coastal waters of the East China Sea:coupled biophysical numerical modeling. Acta Oceanologica Sinica, 36(6):23-33.
Tang Y Z, Gobler C J. 2009. Characterization of the toxicity of Cochlodinium polykrikoides isolates from Northeast US estuaries to finfish and shellfish. Harmful Algae, 8(3):454-462.
Tang Y Z, Gobler C J. 2012. Lethal effects of Northwest Atlantic Ocean isolates of the dinoflagellate, Scrippsiella trochoidea, on Eastern oyster (Crassostrea virginica) and Northern quahog (Mercenaria mercenaria) larvae.Marine Biology, 159(1):199-210.
Tang Y Z, Kong L S, Holmes M J. 2007. Dinoflagellate Alexandrium leei (Dinophyceae) from Singapore coastal waters produces a water-soluble ichthyotoxin. Marine Biology, 150(4):541-549.
Taroncher-Oldenburg G, Kulis D M, Anderson D M. 1997.Toxin variability during the cell cycle of the dinoflagellate Alexandrium fundyense. Limnology and Oceanography, 42(5):1 178-1 188.
Taylor R L, Abrahamsson K, Godhe A, Wängberg S Å. 2009.Seasonal variability in polyunsaturated aldehyde production potential among strains of Skeletonema marinoi (Bacillariophyceae). Journal of Phycology, 45(1):46-53.
Twiner M J, Rehmann N, Hess P, Doucette G J. 2008.Azaspiracid shellfish poisoning:a review on the chemistry, ecology, and toxicology with an emphasis on human health impacts. Marine Drugs, 6(2):39-72.
US Environmental Protection Agency. 1998. EPA Method 556 Determination of carbonyl compounds in drinking water by pentafluorobenzylhidroxylamine derivatization and capillary gas chromatography with electron capture detection. EPA, Cincinatti, OH.
Usup G, Kulis D M, Anderson D M. 1994. Growth and toxin production of the toxic dinoflagellate Pyrodinium bahamense var. compressum in laboratory cultures.Natural Toxins, 2(5):254-262.
Van Wagoner R M, Deeds J R, Tatters A O, Place A R, Tomas C R, Wright J L C. 2010. Structure and relative potency of several karlotoxins from Karlodinium veneficum. Journal of Natural Products, 73(8):1 360-1 365.
Vardi A, Formiggini F, Casotti R, De Martino A, Ribalet F, Miralto A, Bowler C. 2006. A stress surveillance system based on calcium and nitric oxide in marine diatoms.PLoS Biology, 4(3):e60.
Varrella S, Romano G, Ianora A, Bentley M G, Ruocco N, Costantini M. 2014. Molecular response to toxic diatomderived aldehydes in the sea urchin Paracentrotus lividus.Marine Drugs, 12(4):2 089-2 113.
Vidoudez C, Casotti R, Bastianini M, Pohnert G. 2011a.Quantification of dissolved and particulate polyunsaturated aldehydes in the Adriatic Sea. Marine Drugs, 9(4):500-513.
Vidoudez C, Nejstgaard J C, Jakobsen H H, Pohnert G. 2011b.Dynamics of dissolved and particulate polyunsaturated aldehydes in Mesocosms inoculated with different densities of the diatom Skeletonema marinoi. Marine Drugs, 9(3):345-358.
Vidoudez C, Pohnert G. 2008. Growth phase-specific release of polyunsaturated aldehydes by the diatom Skeletonema marinoi. Journal of Plankton Research, 30(11):1 305-1 313.
Wendel T, Jüttner F. 1996. Lipoxygenase-mediated formation of hydrocarbons and unsaturated aldehydes in freshwater diatoms. Phytochemistry, 41(6):1 445-1 449.
Wichard T, Poulet S A, Boulesteix A L, Ledoux J B, Lebreton B, Marchetti J, Pohnert G. 2008. Influence of diatoms on copepod reproduction. Ⅱ. Uncorrelated effects of diatomderived α,β,γ,δ-unsaturated aldehydes and polyunsaturated fatty acids on Calanus helgolandicus in the field. Progress in Oceanography, 77:30-44.
Wichard T, Poulet S A, Halsband-Lenk C, Albaina A, Harris R, Liu D Y, Pohnert G. 2005a. Survey of the chemical defence potential of diatoms:screening of fifty species for α,β,γ,δ-unsaturated aldehydes. Journal of Chemical Ecology, 31(4):949-958.
Wichard T, Poulet S A, Pohnert G. 2005b. Determination and quantification of α,β,γ,δ-unsaturated aldehydes as pentafluorobenzyl-oxime derivates in diatom cultures and natural phytoplankton populations:application in marine field studies. Journal of Chromatography B, 814(1):155-161.
Wu N, Jiang T J, Jiang T. 2012. Analyses of hemolytic toxin from ichthyotoxic phytoplankton Chattonella marina(Hong Kong Strain) by high performance liquid chromatography. Chinese Journal of Analytical Chemistry, 40(8):1 181-1 186. (in Chinese with English abstract)
Xu N, Wang M, Tang Y Z, Zhang Q, Duan S, Gobler C J. 2017.Acute toxicity of the cosmopolitan bloom-forming dinoflagellate Akashiwo sanguinea to finfish, shellfish, and zooplankton. Aquatic Microbial Ecology, 80:209-222.
Yates B S, Rogers W J. 2011. Atrazine selects for ichthyotoxic Prymnesium parvum, a possible explanation for golden algae blooms in lakes of Texas, USA. Ecotoxicology, 20(8):2 003-2 010.
Zhang G T, Sun S. 2004. Effects of diatoms on reproduction and growth of marine copepods. Progress in Natural Science, 14(10):841-847.
Zubía E, Gavagnin M, Crispino A, Martinez E, Ortea J, Cimino G. 1993. Diasteroisomeric ichthyotoxic acylglycerols from the dorsum of two geographically distinct populations of Archidoris nudibranchs. Experientia, 49(3):268-271.
|
|
|
|