Heteroxanthin as a pigment biomarker for Gonyostomum semen (Raphidophyceae)


Autoři: Camilla Hedlund Corneliussen Hagman aff001;  Thomas Rohrlack aff001;  Silvio Uhlig aff002;  Vladyslava Hostyeva aff003
Působiště autorů: Limnology and Hydrology group, Section for Soil and Water, Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, Ås, Norway aff001;  Toxinology Research Group, Norwegian Veterinary Institute, Oslo, Norway aff002;  Norwegian Culture Collection of Algae, Section for Microalgae, Norwegian Institute for Water Research, Oslo, Norway aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226650

Souhrn

The ability to identify drivers responsible for algal community shifts is an important aspect of environmental issues. The lack of long-term datasets, covering periods prior to these shifts, is often limiting our understanding of drivers responsible. The freshwater alga, Gonyostomum semen (Raphidophyceae), has significantly increased distribution and mass occurrences in Scandinavian lakes during the past few decades, often releasing a skin irritating slime that causes discomfort for swimmers. While the alga has been extensively studied, long-term data from individual lakes are often absent or greatly limited and drivers behind this species’ success are still not clear. However, if specific and persistent taxa biomarkers for G. semen could be detected in dated sediment cores, long-term data would be improved and more useful. To test for biomarkers, we examined the pigment composition of several G. semen strains in culture. Further, dated sediment core samples from Lake Lundebyvann, Norway, were used to test the pigments’ suitability as biomarkers in paleolimnological studies. Modifications to a common analysis allowed for the successful detection of the polar xanthophyll heteroxanthin and the non-polar chlorophyll a, as well as several other algal pigments by using high performance liquid chromatography-photometric diode arrays (HPLC-PDA). Heteroxanthin was confirmed by liquid chromatography-mass spectrometry (LC-MS) and detected by HPLC-PDA in all examined G. semen strains, along with chlorophyll a. Using HPLC-PDA, we also identified and confirmed the presence of the biomarker, xanthophyll heteroxanthin, in sediment core samples up to 60 years of age. The specificity of this xanthophyll was also tested by examining a wide range of algal strains from common Norwegian phytoplankton species. Heteroxanthin was not detected in any species commonly occurring in significant amounts in Norwegian lakes. We therefore conclude that heteroxanthin is a suitable pigment biomarker for G. semen and that this pigment can be successfully used for paleolimnological studies.

Klíčová slova:

Algae – Biomarkers – High performance liquid chromatography – Chlorophyll – Lakes – Pigments – Sediment – Semen


Zdroje

1. Sörensen I. Gonyostomum semen (Ehrenb.) Diesing—en vattenorganism av teoretiskt och praktickt intresse. Svensk Faunistisk Revy. 1954;2:6.

2. Bjørndalen K, Løvstad Ø. En regionalundersøkelse av innsjøer i Østfold. Eutrofiering og problemalger. VANN. 1984;1:10.

3. Lepistö L, Antikainen S, Kivinen J. The occurrence of Gonyostomum semen (Ehr.) Diesing in Finnish lakes. Hydrobiologia. 1994;273:1–8.

4. Cronberg G, Lindmark G, Björk S. Mass development of the flagellate Gonyostomum semen (Raphidophyta) in Swedish forest lakes—an effect of acidification? Hydrobiologia. 1988;161:217–36.

5. Hongve D, Løvstad Ø, Bjørndalen K. Gonyostomum semen—a new nuisance to bathers in Norwegian lakes. Verh Internat Verein Limnol. 1988;23:430–4.

6. Hagman CHC, Ballot A, Hjermann DO, Skjelbred B, Brettum P, Ptacnik R. The occurrence and spread of Gonyostomum semen (Ehr.) Diesing (Raphidophyceae) in Norwegian lakes. Hydrobiologia. 2015;744(1):1–14. doi: 10.1007/s10750-014-2050-y WOS:000346182100001.

7. Rengefors K, Weyhenmeyer GA, Bloch I. Temperature as a driver for the expansion of the microalga Gonyostomum semen in Swedish lakes. Harmful Algae. 2012;18:65–73. Epub 25. April 2012.

8. Lebret K, Fernandez MF, Hagman CHC, Rengefors K, Hansson LA. Grazing resistance allows bloom formation and may explain invasion success of Gonyostomum semen. Limnology and Oceanography. 2012;57(3):727–34. doi: 10.4319/lo.2012.57.3.0727 WOS:000306239300005.

9. Lebret K, Ostman O, Langenheder S, Drakare S, Guillemette F, Lindstrom ES. High abundances of the nuisance raphidophyte Gonyostomum semen in brown water lakes are associated with high concentrations of iron. Sci Rep. 2018;8:10. doi: 10.1038/s41598-017-18422-7 WOS:000444022800067.

10. Trigal C, Hallstan S, Johansson KSL, Johnson RK. Factors affecting occurrence and bloom formation of the nuisance flagellate Gonyostomum semen in boreal lakes. harmful Algae. 2013;27:8.

11. Findlay DL, Paterson MJ, Hendzel LL, Kling HJ. Factors influencing Gonyostomum semen blooms in a small boreal reservoir lake. Hydrobiologia. 2005;533:243–52.

12. Johansson KSL, Luhrig K, Klaminder J, Rengefors K. Development of a quantitative PCR method to explore the historical occurrence of a nuisance microalga under expansion. Harmful Algae. 2016;56:67–76. doi: 10.1016/j.hal.2016.04.012 WOS:000379277100007. 28073497

13. Hobaek A, Lovik JE, Rohrlack T, Moe SJ, Grung M, Bennion H, et al. Eutrophication, recovery and temperature in Lake Mjosa: detecting trends with monitoring data and sediment records. Freshwater Biology. 2012;57(10):1998–2014. doi: 10.1111/j.1365-2427.2012.02832.x WOS:000308405300003.

14. Reuss NS, Anderson NJ, Fritz SC, Simpson GL. Responses of microbial phototrophs to late-Holocene environmental forcing of lakes in south-west Greenland. Freshwater Biology. 2013;58(4):690–704. doi: 10.1111/fwb.12073 WOS:000316286700006.

15. Engels S, van Oostrom R, Cherli C, Dungait JAJ, Jansen B, van Aken JM, et al. Natural and anthropogenic forcing of Holocene lake ecosystem development at Lake Uddelermeer (The Netherlands). J Paleolimn. 2018;59(3):329–47. doi: 10.1007/s10933-017-0012-x WOS:000425130600003.

16. Leavitt PR, Hodgson DA. Sedimentary pigments. In: Smol JP, Birks HJB, Kast WM, editors. Tracking Environmental Change Using Lake Sediments: Terrestrial, Algal, and Siliceous Indicators. 3. Dordrecht, The Netherlands: Kluwer Academic Publishers; 2001. p. 295–325.

17. Millie DF, Paerl HW, Hurley JP. Microalgal pigment assessments using High-Performance Liquid-Chromatography—A synopsis of organismal and ecological applications. Can J Fish Aquat Sci. 1993;50(11):2513–27. doi: 10.1139/f93-275 WOS:A1993MZ45600023.

18. Ellegaard M, Clarke AL, Reuss N, Drew S, Weckstrom K, Juggins S, et al. Multi-proxy evidence of long-term changes in ecosystem structure in a Danish marine estuary, linked to increased nutrient loading. Estuar Coast Shelf Sci. 2006;68(3–4):567–78. doi: 10.1016/j.ecss.2006.03.013 WOS:000238871700020.

19. Gieskes WWC, Kraay GW. Dominance of Cryptophyceae during the phytoplankton spring bloom in the central North-Sea detected by HPLC analysis of pigments. Mar Biol. 1983;75(2–3):179–85. doi: 10.1007/bf00406000 WOS:A1983RG96900009.

20. Chapman DJ, Haxo F. Chloroplast pigments of Chloromonadophyceae. Journal of Phycology. 1966;2(2):89–91. doi: 10.1111/j.1529-8817.1966.tb04599.x 27053320

21. Guillard RRL, Lorenzen CJ. Yellow-green algae with chlorophyllide c. J Phycol. 1972;8:10–4.

22. Fiksdahl A, Withers N, Guillard RRL, Liaaenjensen S. Carotenoids of the Raphidophyceae—a chemosystematic contribution. Comp Biochem Physiol B-Biochem Mol Biol. 1984;78(1):265–71. doi: 10.1016/0305-0491(84)90181-0 WOS:A1984SV19800046.

23. Sassenhagen I, Rengefors K, Richardson TL, Pinckney JL. Pigment composition and photoacclimation as keys to the ecological success of Gonyostomum semen (Raphidophyceae, Stramenopiles). J Phycol. 2014;50:9.

24. Chapman DJ. Three new carotenoids isolated from algae. Phytochemistry. 1966;5(6):1331–3. https://doi.org/10.1016/S0031-9422(00)86131-2.

25. Kleinig H, Egger K. Carotinoide der Vaucheriales Vaucheria und Botrydium (Xanthophyceae). Zeitschrift Fur Naturforschung Part B-Chemie Biochemie Biophysik Biologie Und Verwandten Gebiete. 1967;B 22(8):868–&. WOS:A19679866500015.

26. Strain HH, Svec WA, Aitzetmuller K, Grandolfo M, Katz JJ. Molecular weights and empirical formulas of Xanthophylls of Vaucheria. Phytochemistry. 1968;7(8):1417–+. doi: 10.1016/s0031-9422(00)85649-6 WOS:A1968B447400034.

27. Strain HH, Benton FL, Grandolfo MC, Aitzetmueller K, Svec WA, Katz JJ. Heteroxanthin, diatoxanthin and diadinoxanthin from Tribonema aequale. Phytochemistry. 1970;9(12):2561–+. doi: 10.1016/s0031-9422(00)85778-7 WOS:A1970I161800022.

28. Nitsche H. Heteroxanthin in Euglena gracilis. Arch Mikrobiol. 1973;90(2):151–5. doi: 10.1007/bf00414517 4196487

29. Andersen RA, Potter D, Bidigare RR, Latasa M, Rowan K, O'Kelly CJ. Characterization and phylogenetic position of the enigmatic golden alga Phaeothamnion confervicola: Ultrastructure, pigment composition and partial SSU rDNA sequence. Journal of Phycology. 1998;34(2):286–98. doi: 10.1046/j.1529-8817.1998.340286.x WOS:000073239700012.

30. Bailey JC, Bidigare RR, Christensen SJ, Andersen RA. Phaeothamniophyceae classis nova: A new lineage of chromophytes based upon photosynthetic pigments, rbcL sequence analysis and ultrastructure. Protist. 1998;149(3):245–63. doi: 10.1016/S1434-4610(98)70032-X WOS:000076195000005. 23194637

31. Xiao Y, Rohrlack T, Riise G. Unraveling long-term changes in lake color based on optical properties of lake sediment. Science of The Total Environment. 2019:134388. https://doi.org/10.1016/j.scitotenv.2019.134388.

32. Wright SW, Jeffrey SW, Mantoura RFC, Llewellyn CA, Bjornland T, Repeta D, et al. Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol-Prog Ser. 1991;77(2–3):183–96. doi: 10.3354/meps077183 WOS:A1991GV75600008.

33. Buchecker R, Liaaen-Jensen S. Absolute configuration of heteroxanthin and diadinoxanthin. Phytochemistry. 1977;16(6):729–33. doi: 10.1016/s0031-9422(00)89242-0 WOS:A1977DF76600024.

34. Guaratini T, Vessecchi RL, Lavarda FC, Campos P, Naal Z, Gates PJ, et al. New chemical evidence for the ability to generate radical molecular ions of polyenes from ESI and HR-MALDI mass spectrometry. Analyst. 2004;129(12):1223–6. doi: 10.1039/b412154f WOS:000225335500012. 15565222

35. Norwegian Environment Agency. Vannmiljø [26.07.2019]. Available from: https://vannmiljo.miljodirektoratet.no.

36. Rohrlack T, Haaland S. Paleolimnologisk undersøkelse av Lundebyvannet i Eidsberg kommune. Ås, Norway: Norwegian University of Life Sciences, 2017.

37. Haande S, Edvardsen H, Eriksen T, Kile M, Hagman CHC, Borch H, et al. Tilstandsklassifisering av vannforekomster i Vannområde Glomma Sør for Øyeren (2011) i henhold til vannforskriften. Norwegian Institute for Water Research: 2012.

38. Stabell T. Klassifisering av innsjøer i Vannområde Glomma sør for Øyeren etter kvalitetselementet «planteplankton». Datarapport, 2018. FAUN, 2019.

39. AlgaeBase. algaebase.org [02.06.2019]. Available from: http://www.algaebase.org/.


Článek vyšel v časopise

PLOS One


2019 Číslo 12