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Effects of prolonged darkness and temperature on the lipid metabolism in the benthic diatom Navicula perminuta from the Arctic Adventfjorden, Svalbard

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Abstract

The Arctic represents an extreme habitat for phototrophic algae due to long periods of darkness caused by the polar night (~4 months darkness). Benthic diatoms, which dominate microphytobenthic communities in shallow water regions, can survive this dark period, but the underlying physiological and biochemical mechanisms are not well understood. One of the potential mechanisms for long-term dark survival is the utilisation of stored energy products in combination with a reduced basic metabolism. In recent years, water temperatures in the Arctic increased due to an ongoing global warming. Higher temperatures could enhance the cellular energy requirements for the maintenance metabolism during darkness and, therefore, accelerate the consumption of lipid reserves. In this study, we investigated the macromolecular ratios and the lipid content and composition of Navicula cf. perminuta Grunow, an Arctic benthic diatom isolated from the microphytobenthos of Adventfjorden (Svalbard, Norway), over a dark period of 8 weeks at two different temperatures (0 and 7 °C). The results demonstrate that N. perminuta uses the stored lipid compound triacylglycerol (TAG) during prolonged dark periods, but also the pool of free fatty acids (FFA). Under the enhanced temperature of 7 °C, the lipid resources were used significantly faster than at 0 °C, which could consequently lead to a depletion of this energy reserves before the end of the polar night. On the other hand, the membrane building phospho- and glycolipids remained unchanged during the 8 weeks darkness, indicating still intact thylakoid membranes. These results explain the shorter survival times of polar diatoms with increasing water temperatures during prolonged dark periods.

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Abbreviations

Cer:

Ceramide

CH:

Carbohydrates

Chol:

Cholesterol

DAG:

Diacylglycerole

DGCC:

Diacylglycerylcarboxyhydroxymethyl-choline

DGDG:

Digalactosyldiacylglycerols

DM:

Dry mass

Eb:

Ester bond

FA:

Fatty acids

FAME:

Fatty acid methyl esters

FFA:

Free fatty acids

FTIR:

Fourier transform infrared

GC–MS:

Gas chromatography–mass spectrometry

HPLC:

High-pressure liquid chromatography

IS:

Internal standard

LPC:

Lysophosphatidylcholine

MD:

Mean deviation from the median

MGDG:

Monogalactosyldiacylglycerols

MPB:

Microphytobenthos

MS:

Mass spectrometry

MUFA:

Monounsaturated fatty acids

PC:

Phosphatidylcholine

PE:

Phosphatidylethanolamine

PG:

Phosphatidylglycerols

PI:

Phosphatidylinositole

PS:

Phosphatidylserine

PUFA:

Polyunsaturated fatty acids

SFA:

Saturated fatty acids

Si:

Silicate

SQDG:

Sulphoquinovosyldiacylglycerols

TAG:

Triacylglycerols

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Acknowledgements

The work on microphytobenthos has been performed at the Ny-Ålesund International Arctic Environmental Research and Monitoring Facility and under the agreement on scientific cooperation between the Alfred Wegener Institute and the University of Rostock. The authors thank the crew at the AWIPEV-base in Ny-Ålesund and the German dive team (Anita Flohr, Peter Leopold, Max Schwanitz) for assistance in the field, collecting samples and further support. We thank Nadine Dolata for isolating the investigated diatom species and Juliane Müller for maintaining the stock collection of Arctic benthic diatoms at the University of Rostock. Furthermore, we thank Dr. Dieter Janssen (Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Ecological Chemistry) for HPLC calibration and measurements. Thanks to Dr. Susann Schaller-Laudel (University of Leipzig, Institute of Biology, Plant Physiology) for providing plant lipid standards from Lipid Products, England. Financial and logistic support of the microphytobenthic research was provided by the German Research Council to UK in the frame of the Deutsche Forschungsgemeinschaft (DFG) priority program 1158 “Antarctic Research” (DFG, KA899/12, KA899/15). In addition, the FTIR measurements were supported by DFG grants from Prof. C. Wilhelm (Wi64/10, Wi64/14, Wi64/19).

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Schaub, I., Wagner, H., Graeve, M. et al. Effects of prolonged darkness and temperature on the lipid metabolism in the benthic diatom Navicula perminuta from the Arctic Adventfjorden, Svalbard. Polar Biol 40, 1425–1439 (2017). https://doi.org/10.1007/s00300-016-2067-y

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