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Diurnal effects of anoxia on the metabolome of the seagrass Zostera marina

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Abstract

We investigated the response, adaptation and tolerance mechanisms of the temperate seagrass Zostera marina to water column anoxia. We exposed Z. marina to a diurnal light/dark cycle under anoxia and assessed the metabolic response by measuring the metabolome with gas chromatography coupled to mass spectrometry (GC–MS). During anoxia and light exposure the roots showed an altered metabolome whereas the leaves were only marginally affected, indicating that photosynthetically derived oxygen could satisfy the oxygen demand in the leaves but not in the roots. Nocturnal anoxia caused a biphasic shift in the metabolome of roots and leaves. The first phase, after 15 h under anoxia and 3 h of darkness showed a fast increase of lactate, pyruvate, GABA (γ-aminobutyric acid), succinate, alanine and a decrease in glutamate and glutamine. The second phase, after 21 h under anoxia and 9 h of darkness showed a decrease in lactate and pyruvate and an increase in alanine, GABA and succinate. This reprogramming of the metabolome after 21 h under anoxia indicates a possible mitigation mechanism to avoid the toxic effects of anoxia. A pathway enrichment analysis proposes the alanine shunt, the GABA shunt and the 2-oxoglutarate shunt as such mitigation mechanisms that alleviate pyruvate levels and lead to carbon and nitrogen storage during anoxia. This work demonstrates the applicability of metabolomics to assess low oxygen stress responses of Z. marina and allows us to propose an anoxia recovery model.

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Acknowledgments

Thanks to the staff of the eco-lab at the University of Southern Denmark for assistance in sample analysis of nutrients. We are in depth of Raymond P. Cox for proof-reading and editing this papers and also of Zeljko Jovanovic for his help during the initial preparations of the experiment. We thank the anonymous reviewers for their valuable comments. Harald Hasler-Sheetal was funded by the Danish Council of Independent Research (Grant No. 09-067485) and Marianne Holmer from Danish National Research foundation (Grant No. 12-127012).

Conflict of interest

H. Hasler-Sheetal, L. Fragner, M. Holmer and W. Weckwerth declare that they have no conflict of interest.

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  1. Department of Biology, University of Southern Denmark, Campusvej 52, 5230, Odense M, Denmark

    Harald Hasler-Sheetal & Marianne Holmer

  2. Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria

    Lena Fragner & Wolfram Weckwerth

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  1. Harald Hasler-Sheetal
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Hasler-Sheetal, H., Fragner, L., Holmer, M. et al. Diurnal effects of anoxia on the metabolome of the seagrass Zostera marina . Metabolomics 11, 1208–1218 (2015). https://doi.org/10.1007/s11306-015-0776-9

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