Contemporary Problems of Ecology

, Volume 11, Issue 2, pp 179–194 | Cite as

Interannual Variability of Low-Molecular Metabolite Composition in Ceratophyllum demersum (Ceratophyllaceae) from a Floodplain Lake with a Changeable Trophic Status

  • E. A. Kurashov
  • G. G. Mitrukova
  • J. V. Krylova
Article

Abstract

The regularities that shape the composition of low molecular weight organic compounds (LMWOCs) in aquatic macrophytes in response to aquatic environment alterations remain poorly characterized. The aim of the present study consists of a comparative interannual investigation into LMWOC composition in rigid hornwort (Ceratophyllum demersum L.) from a Volga-Akhtuba floodplain lake with a variable trophic state. A high variability of LMWOC composition and individual compound levels in hornwort is detected as different trophic states of the water body are analyzed. Active allelochemicals are the predominant LMWOCs in the case of a “macrophytic” mesotrophic state of the lake, with fatty acids (the free fatty acid fraction) apparently being the most important in this group. Hornwort LMWOC composition in the case of a “cyanobacterial” eutrophic type of lake development is characterized by the predomination of compounds that enhance the protective reactions (manool being the most important) under the conditions of suppression by cyanobacteria, which is also manifested as an almost twofold decrease in the overall intensity of organiccompound biosynthesis.

Keywords

Ceratophyllum demersum cyanobacteria macrophytes low molecular weight organic compounds gas chromatography–mass spectrometry allelopathy low molecular weight metabolome 

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References

  1. Achotegui-Castells, A., Danti, R., Liusià, J., Della Rocca, G., Barberini, S., and Peñuelas, J., Strong induction of minor terpenes in Italian cypress, Cupressus sempervirens, in response to infection by the fungus Seiridium cardinale, J. Chem. Ecol., 2015, vol. 41, pp. 224–243. doi 10.1007/s10886-015-0554-1CrossRefPubMedGoogle Scholar
  2. Ahel, M., McEvoy, J., and Giger, W., Bioaccumulation of the lipophilic metabolites of nonionic surfactants in fresh-water organisms, Environ. Pollut., 1993, vol. 79, pp. 243–248.CrossRefPubMedGoogle Scholar
  3. Alekin, O.A., Semenov, A.D., and Skopintsev, B.A., Rukovodstvo po khimicheskomu analizu vod sushi (Manual on Chemical Analysis of Inland Waters), Leningrad: Nauka, 1973.Google Scholar
  4. Anderson, P.M., Hilker, M., Hansson, B.S., Bombosch, S., Klein, B., and Schildknecht, H., Oviposition deterring components in larval frass of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae): a behavioral and electrophysiological evaluation, J. Insect Physiol., 1993, vol. 39, pp. 129–137.CrossRefGoogle Scholar
  5. Blackburn, M.A., Kirby, S.J., and Waldock, M.J., Concentrations of alkyphenol polyethoxylates entering UK estuaries, Mar. Pollut. Bull., 1999, vol. 38, no. 2, pp. 109–118.CrossRefGoogle Scholar
  6. Carlson, R.E., A trophic state index for lakes, Limnol. Oceanogr., 1977, vol. 22, no. 2, pp. 361–369.CrossRefGoogle Scholar
  7. Bul’on, V.V., Pervichnaya produktsiya planktona vnutrennikh vodoemov (Primary Production of Plankton of Inland Reservoirs), Leningrad: Nauka, 1983.Google Scholar
  8. Burakovskii, A.I., Piven’, N.V., and Lukhverchik, L.N., Nonylphenol as a damaging factor in the regulatory systems of the organism, Tr. Beloruss. Gos. Univ., Farmakol. Farm., 2010, vol. 5, no. 1, pp. 243–254.Google Scholar
  9. Bykova, S.N., Borisovskaya, E.V., and Vinogradov, G.A., Influence of some macrophytes and filamentous green alga on succession of microperiphyton communities, Povolzhsk. Ekol. Zh., 2010, no. 3, pp. 241–253.Google Scholar
  10. Czekanowski, J., Coefficient of racial likeness und Durchschnittliche Differenz, Anthropol. Anz., 1922, vol. 9, pp. 227–249.Google Scholar
  11. Demetzos, C. and Dimas, K.S., Labdane-type diterpenes: chemistry and biological activity, Stud. Nat. Prod. Chem., 2001, vol. 25, pp. 235–292.CrossRefGoogle Scholar
  12. Dmitriev, V.V., Myakisheva, N.V., Tret’yakov, V.Yu., and Khovanov, N.V., Multicriteria evaluation of ecological status and stability of geological systems based on the method of aggregated indicators, II. Trophic status of aquatic ecosystems, Vestn. S.-Peterb. Univ., Ser. 7: Geol., Geogr., 1997, vol. 1, no. 7, pp. 51–67.Google Scholar
  13. Du, Z.Y. and Benning, C., Triacylglycerol accumulation in photosynthetic cells in plants and algae, in Lipids in Plant and Algae Development, Nakamura, Y. and Li-Beisson, Y., Eds., New York: Springer-Verlag, 2016, pp. 179–205. doi 10.1007/978-3-319-25979-6_8CrossRefGoogle Scholar
  14. Dubyna, D.V., Stoiko, S.M., Sytnik, K.M., Tasenkevich, L.A., Shelyag-Sosonko, Yu.R., Geiny, S., Groudova, Z., Gusak, Sh., Otyagelova, G., and Erzhabkova, O., Makrofity—indikatoryizmenenii prirodnoi sredy (Macrophytes as the Indicators of Environmental Changes), Kiev: Naukova Dumka, 1993.Google Scholar
  15. Ekeberg, D., Jablonska, A.M., and Ogner, G., Phytol as a possible indicator of ozone stress by Picea abies, Environ. Pollut., 1995, vol. 89, pp. 55–58.CrossRefGoogle Scholar
  16. Ekelund, R., Bergman, A., Granmo, A., and Berggre, M., Bioaccumulation of 4-nonylphenol in marine animals. A re-evaluation, Environ. Pollut., 1990, no. 64, pp. 107–120.CrossRefPubMedGoogle Scholar
  17. Filippov, O.V., Kochetkova, A.I., Baranova, M.S., and Bryzgalina, E.S., Modern status and problems of water consumption in Volga-Akhtuba floodplain, Grani Poznaniya, 2015, no. 4 (38), pp. 31–41.Google Scholar
  18. Fink, P., Ecological functions of volatile organic compounds in aquatic systems, Mar. Freshwater Behav. Physiol., 2007, vol. 40, no. 3, pp. 155–168.CrossRefGoogle Scholar
  19. Fitoplnkton Nizhnei Volgi. Vodokhranilishcha i nizov’e reki (Phytoplankton of Lower Volga. Reservoirs and River Lower Reaches), Trifonov, I.S., Ed., St. Petersburg: Nauka, 2003.Google Scholar
  20. Gening, V.F., Bunyatyan, E.P., Pustovalov, S.Zh., and Rychkov, N.A., Formalizaovanno-statisticheskie metody v arkheologii (analiz pogrebal’nykh pamyatnikov) (Formalized Statistical Methods Applied in Archeology: Analysis of Buried Monuments), Kiev: Naukova Dumka, 1990.Google Scholar
  21. GOST (State Standard) 24027.2-80: Methods for Determination of Moisture, Ash Content, Extractive, and Tannin Materials, Essential Oil, Moscow: Izd. Standartov, 1980.Google Scholar
  22. GOST (State Standard) 17082.4-88: Fruits of Ethereal-Oil Crops. Industrial Raw Material. Methods for Determination of Essential Oil Mass Fraction, Moscow: Izd. Standartov, 1989}, pp. 13–24Google Scholar
  23. Gosudarstvennyi doklad o sostoyanii prirodnykh resursov i okhrane okruzhayushchei sredy Astrakhanskoi oblasti za 2009 god (The State Report of the Natural Resources and Protection of Environment in Astrakhan Oblast in 2009), Astrakhan, 2010.Google Scholar
  24. Gurevich, F.A., Role of phytoncides in inland reservoirs, Vodn. Resur., 1978, no. 2, pp. 133–142.Google Scholar
  25. Hanari, N., Yamamoto, H., and Kuroda, K., Comparison of terpenes in extracts from the resin and the bark of the resinous stem canker of Chamaecyparis obtuse and Thujopsis dolabrata var. hondae, J. Wood. Sci., 2002, vol. 48, no. 1, pp. 56–63.CrossRefGoogle Scholar
  26. Hu, H. and Hong, Y., Algal-bloom control by allelopathy of aquatic macrophytes—a review, Front. Environ. Sci. Eng. China, 2008, vol. 2, no. 4, pp. 421–438.CrossRefGoogle Scholar
  27. Islam, M.T., De Alencar, M.V.O.B., Da Conceição Machado, K., Da Conceição Machado, K., De Carvalho Melo-Cavalcante, A.A., De Sousa, D.P., and De Freitas, R.M., Phytol in a pharma-medico-stance, Chem.-Biol. Interact., 2015, vol. 240, pp. 60–73.CrossRefPubMedGoogle Scholar
  28. Jaccard, P., Distribution de la flore alpine dans le bassin des Dranses et dans quelques régions voisines, Bull. Soc. Vaudoise Sci. Nat., 1901, vol. 37, no. 140, pp. 241–272.Google Scholar
  29. Jackson, L.J., Macrophyte-dominated and turbid states of shallow lakes: evidence from Alberta lakes, Ecosystems, 2003, vol. 6, pp. 213–223. doi 10.1007/s10021-002-0001-3CrossRefGoogle Scholar
  30. Jüttner, F., Nor-carotenoids as the major volatile excretion products of Cyanidium, Z. Naturforsch., C, 1979, vol. 34, pp. 186–191.Google Scholar
  31. Kim, J.W., Huh, J.E., Kyung, S.H., and Kyung, K.H., Antimicrobial activity of alk(en)yl sulfides found in essential oils of garlic and onion, Food Sci. Biotechnol., 2004, vol. 13, no. 2, pp. 235–239.Google Scholar
  32. Kitaev, S.P., Osnovy limnologii dlya gidrobiologov i ikhtiologov (Basic Limnology for Hydrobiologists and Ichthyologists), Petrozavodsk: Karel. Nauch. Tsentr, Ross. Akad. Nauk, 2007.Google Scholar
  33. Krylova, Yu.V., Kurashov, E.A., and Mitrukova, G.G., Components of volatile low-molecular organic compounds of Ceratophyllu demersum (Ceratophyllaceae) growing in various climatic conditions, Voda: Khim. Ekol., 2016, no. 8, pp. 11–24.Google Scholar
  34. Kurashov, E.A., Krylova, Yu.V., and Mitrukova, G.G., Composition of volatile low-molecular organic substances of Ceratophyllum demersum L. during fruiting, Voda: Khim. Ekol., 2012, no. 6, pp. 107–116.Google Scholar
  35. Kurashov, E.A., Krylova, J.V., Mitrukova, G.G., and Chernova, A.M., Low-molecular-weight metabolites of aquatic macrophytes growing on the territory of Russia and their role in hydroecosystems, Contemp. Probl. Ecol., 2014, vol. 7, no. 4, pp. 433–448.CrossRefGoogle Scholar
  36. Kurashov, E.A., Bataeva, Yu.V., Krylova, Yu.V., and Mitrukova, G.G., Biosynthesis of low-molecular organic compounds by aquatic macrophytes and cyanobacteria and their prospective use, in Biotekhnologiya: sostoyanie i perspektivy razvitiya (Biotechnology: Current Status and Prospective Development), Moscow: Ross. Khim.-Tekhnol. Univ. im. D.I. Mendeleeva, 2015, pp. 332–333.Google Scholar
  37. Kurashov, E.A., Fedorova, E.V., Krylova, J.V., and Mitrukova, G.G., Assessment of the potential biological activity of low molecular weight metabolites of freshwater macrophytes with QSAR, Scientifica, 2016, vol. 2016, art. ID 1205680. doi 10.1155/2016/1205680Google Scholar
  38. Lamikanra, O. and Richard, O.A., Effect of storage on some volatile aroma compounds in fresh-cut cantaloupe melon, J. Agric. Food Chem., 2002, vol. 50, pp. 4043–4047.CrossRefPubMedGoogle Scholar
  39. Lee, L.S. Brooks, L.O., Homer, L.E., Rossetto, M., Henry, R.J., and Baverstock, P.R., Geographic variation in the essential oils and morphology of natural populations of Melaleuca alternifolia (Myrtaceae), Biochem. Syst. Ecol., 2002, vol. 30, no. 4, pp. 343–360.CrossRefGoogle Scholar
  40. Liorens, L., Liorens-Molina, J.A., Agnello, S., and Boira, H., Geographical and environment-related variations of essential oils in isolated populations of Thymus richardii Pers. in the Mediterranean basin, Biochem. Syst. Ecol., 2014, vol. 56, pp. 246–254. doi 10.1016/j.bse.2014.05.007CrossRefGoogle Scholar
  41. Meteiko, T.Ya., Metabolites of higher aquatic plants and their role in hydrobiocenosises: a review, Gidrobiol. Zh., 1978, vol. 12, no. 4, pp. 3–14.Google Scholar
  42. Metodicheskie rekomendatsii po sboru i obrabotke materialov pri gidrobiologicheskikh issledovaniyakh na presnovodnykh vodoemakh. Fitoplankton i ego produktsiya (Procedure for Collection and Treatment of Materials for Hydrobiological Studies in Freshwater Reservoirs. Phytoplankton and Its Production), Leningrad, 1981.Google Scholar
  43. Milius, A., Concentration of chlorophyll a in phytoplankton of small different-type lakes of Estonia, Izv. Akad. Nauk EstSSR, Biol., 1981, vol. 30, no. 2, pp. 147–157.Google Scholar
  44. Nakai, S., Yamada, S., and Hosomi, M., Anti-cyanobacterial fatty acids released from Myriophyllum spicatum, Hydrobiologia, 2005, vol. 543, pp. 71–78.CrossRefGoogle Scholar
  45. Norris, S., Lincoln, K., Abad, M., Scott, M., Eilers, R., Hartsuyker, K., Kindle, K., Hirshberg, J., Karunanandaa, B., Moshiri, F., Stein, J.C., Valentin, H.E., and Venkatesh, T.V., WO Patent 2 004 013 312 A2, 2004.Google Scholar
  46. Novikov, Yu.V., Lastochkina, K.O., and Boldina, Z.N., Metody issledovaniya kachestva vody vodoemov (Manual for Analysis of Water Quality in Reservoirs), Moscow: Meditisna, 1990.Google Scholar
  47. Nürnberg, G.K., Trophic state of clear and colored, softand hard water lakes with special consideration of nutrients, anoxia, phytoplankton and fish, Lake Reservoir Manage., 1996, vol. 12, no. 4, pp. 432–447. doi 10.1080/07438149609354283CrossRefGoogle Scholar
  48. Peisker, C., Düggelin, T., Rentsch, D., and Matile, P., Phytol and the breakdown of chlorophyll in senescent leaves, J. Plant Physiol., 1989, vol. 135, pp. 428–432.CrossRefGoogle Scholar
  49. Preuss, T.G., Gehrhardt, J., Schirmer, K., Coors, A., Rubach, M., Russ, A., Jones, P.D., Giesy, J.P., and Ratte, H.T., Nonylphenol isomers differ in estrogenic activity, Environ. Sci. Technol., 2006, vol. 40, no. 16, pp. 5147–5153.CrossRefPubMedGoogle Scholar
  50. Pyrina, I.L., Oxidative analysis of primary production of phytoplankton, in Metodicheskie voprosy izucheniya produktsii planktona vnutrennikh vodoemov (Manual for Analysis of Plankton Production in Inland Reservoirs), St. Petersburg: Gidrometeoizdat, 1993, pp. 10–13.Google Scholar
  51. Rukovodstvo po metodam gidrobiologicheskogo analiza poverkhnostnykh vod i donnykh otlozhenii (Manual for Hydrobiological Analysis of Surface Waters and Bottom Sediments), Leningrad: Gidrometeoizdat, 1983.Google Scholar
  52. Santos, S.A.O., Oliveira, C.S.D., Trindade, S.S., Abreu, M.H., Rocha, S.S.M., and Silvestre, A.J.D., Bioprospecting for lipophilic-like components of five Phaeophyta macroalgae from the Portuguese coast, J. Appl. Phycol., 2016, vol. 28, no. 5, pp. 3151–3158. doi 10.1007/s10811-016-0855-yCrossRefGoogle Scholar
  53. Santos, S.A.O., Vilela, C., Freire, C.S.R., Abreu, M.H., Rocha, S.S.M., and Silvestre, A.J.D., Chlorophyta and Rhodophyta macroalgae: a source of health promoting phytochemicals, Food Chem., 2015, vol. 183, pp. 122–128.CrossRefPubMedGoogle Scholar
  54. Scheffer, M., Alternative attractors of shallow lakes, Sci. World, 2001, vol. 1, pp. 254–263. doi 10.1100/tsw.2001.62CrossRefGoogle Scholar
  55. Scheffer, M., Hosper, S.H., Meijer, M.-L., Moss, B., and Jeppesen, E., Alternative equilibria in shallow lakes, Trends Ecol. Evol., 1993, vol. 8, pp. 275–279.CrossRefPubMedGoogle Scholar
  56. Scheffer, M., Carpenter, S., Foley, J.A., Folke, C., and Walker, B., Catastrophic shifts in ecosystems, Nature, 2001, vol. 413, pp. 591–596.CrossRefPubMedGoogle Scholar
  57. Sellami, I.H., Rebey, I.B., Sriti, J., Rahali, F.Z., Limam, F., and Marzouk, B., Drying sage (Salvia officinalis L.) plants and its effects on content, chemical composition and radical scavenging activity of the essential oil, Food Bioprocess Technol., 2012, vol. 5, no. 8, pp. 2978–2989.CrossRefGoogle Scholar
  58. Sfriso, A., Pavoni, B., Marcomini, A., and Orio, A.A., Macroalgae, nutrient cycles, and pollutants in the Lagoon of Venice, Estuaries, 1992, vol. 15, no. 4, pp. 517–528.CrossRefGoogle Scholar
  59. Soares, A., Guieysse, B., Jefferson, B., Cartmell, E., and Lester, J.N., Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters, Environ. Int., 2008, vol. 34, pp. 1033–1049.CrossRefPubMedGoogle Scholar
  60. Sorensen, T.A., A method of establishing groups of equal amplitude in plant sociology based on similarity of species content, and its application to analyses of the vegetation on Danish commons, K. Dan. Vidensk. Selsk. Biol. Skr., 1948, vol. 5, pp. 1–34.Google Scholar
  61. Souza, A.B., De Souza, M.G.M., Moreira, M.A., Moreira, M.R., Furtado, N.A.J.C., Martins, C.H.G., Bastos, J.K., Dos Santos, R.A., Heleno, V.C.G., Ambrosio, S.R., and Veneziani, R.C.S., Antimicrobial evaluation of diterpenes from Copaifera langsdorffii oleoresin against periodontal anaerobic bacteria, Molecules, 2011, vol. 16, no. 11, pp. 9611–9619.CrossRefPubMedGoogle Scholar
  62. Srinivasan, R., Devi, K.R., Kannappan, A., Pandian, S.K., and Ravi, A.V., Piper beetle and its bioactive metabolite phytol mitigates quorum sensing mediated virulence factors and biofilm of nosocomial pathogen Serratia marcescens in vitro, J. Ethnopharmacol., 2016, vol. 193, pp. 592–603.CrossRefPubMedGoogle Scholar
  63. Sun, X., Jin, H., Zhang, L., Hu, W., Li, Y., and Xu, N., Screening and isolation of the algicidal compounds from marine green alga Ulva intestinalis, Chin. J. Ocean. Limnol., 2016, vol. 34, pp. 781–788. doi 10.1007/ s00343-016-4383-zCrossRefGoogle Scholar
  64. Tkachev, A.V., Issledovanie letuchikh veshchestv rastenii (Analysis of Volatile Substances of the Plants), Novosibirsk: Ofset, 2008.Google Scholar
  65. Topçu, G. and Gören, A.G., Biological activity of diterpenoids isolated from Anatolian Lamiaceae plants, Rec. Nat. Prod., 2007, vol. 1, no. 1, pp. 1–16.CrossRefGoogle Scholar
  66. Ulubelen, A., Topçu, G., Eris, C., Sönmez, U., Kartal, M., Kurucu, S., and Bozok-Johansson, C., Terpenoids from Salvia sclarea, Phytochemistry, 1994, vol. 36, pp. 971–974.CrossRefPubMedGoogle Scholar
  67. Valentin, H.E., and Qungang, Q., Tocochromanols: biological function and recent advances to engineer plastidial biochemistry for enhanced oil seed vitamin E levels, in The Chloroplast. Advances in Photosynthesis and Respiration, Rebeiz, C.A., Benning, C., Bohnert, H.J., Daniell, H., Hoober, J.K., Lichtenthaler, H.K., Portis, A.R., and Tripathy, B.C., Eds., Dordrecht: Springer-Verlag, 2010, vol 31, pp. 155–170.CrossRefGoogle Scholar
  68. Vencl, F.V. and Morton, T.C., The shield defense of the sumac flea beetle, Blepharida rhois (Chrysomelidae: Alticinae), Chemoecology, 1998, vol. 8, pp. 25–32.CrossRefGoogle Scholar
  69. Vinberg, G.G., Pervichnaya produktsiya vodoemov (Primary Production of Reservoirs), Minsk, 1960.Google Scholar
  70. Watson, S.B., Cyanobacterial and eukaryotic algal odor compounds: signals or by-products? A review of their biological activity, Phycologia, 2003, vol. 42, no. 4, pp. 332–350.CrossRefGoogle Scholar
  71. Watson, S.B., Caldwell, G., and Pohnert, G., Fatty acids and oxylipins as semiochemicals, in Lipids in Aquatic Ecosystems, Dordrecht: Springer-Verlag, 2009, pp. 65–91.CrossRefGoogle Scholar
  72. Zhang, K., Lin, T.F., Zhang, T., Li, C., and Gao, N., Characterization of typical taste and odor compounds formed by Microcystis aeruginosa, J. Environ. Sci., 2013a, vol. 25, no. 8, pp. 1539–1548.CrossRefGoogle Scholar
  73. Zhang, H., Mallik, A., and Zeng, R.S., Control of Panama disease of banana by rotating and intercropping with Chinese chive (Allium tuberosum Rottler): role of plant volatiles, J. Chem. Ecol., 2013b, vol. 39, no. 2, pp. 243–252. doi 10.1007/s10886-013-0243-xCrossRefPubMedGoogle Scholar
  74. Zuo, S., Zhou, S., Ye, L., Ding, Y., and Jiang, X., Antialgal effects of five individual allelochemicals and their mixtures in low level pollution conditions, Environ. Sci. Pollut. Res., 2016, vol. 23, pp. 15703–15711. doi 10.1007/s11356-016-6770-6CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • E. A. Kurashov
    • 1
    • 4
  • G. G. Mitrukova
    • 1
    • 3
  • J. V. Krylova
    • 2
    • 4
  1. 1.Institute of LimnologyRussian Academy of SciencesSt. PetersburgRussia
  2. 2.Berg State Research Institute of Lake and River FisheriesSt. PetersburgRussia
  3. 3.Saint Petersburg State Chemicopharmaceutical AcademySt. PetersburgRussia
  4. 4.ITMO UniversitySt. PetersburgRussia

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