Transcriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipids

Abstract Background Nutritional quality of phytoplankton is a major determinant of the trophic transfer efficiency at the plant-herbivore interface in freshwater food webs. In particular, the phytoplankton’s content of the essential polyunsaturated omega-3 fatty acid eicosapentaenoic acid (EPA) has...

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Main Authors: Heidrun S. Windisch, Patrick Fink
Format: Article
Language:English
Published: BMC 2019-11-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-019-6268-y
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spelling doaj-d62a560600b64e2991181163d345f0712020-11-25T04:03:18ZengBMCBMC Genomics1471-21642019-11-0120111510.1186/s12864-019-6268-yTranscriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipidsHeidrun S. Windisch0Patrick Fink1Heinrich-Heine-University, Institute for Cell Biology and ZoologyInstitute for Zoology, University of CologneAbstract Background Nutritional quality of phytoplankton is a major determinant of the trophic transfer efficiency at the plant-herbivore interface in freshwater food webs. In particular, the phytoplankton’s content of the essential polyunsaturated omega-3 fatty acid eicosapentaenoic acid (EPA) has been repeatedly shown to limit secondary production in the major zooplankton herbivore genus Daphnia. Despite extensive research efforts on the biological model organism Daphnia, and the availability of several Daphnia genomes, little is known regarding the molecular mechanisms underlying the limitations in Daphnia related to dietary EPA availability. Results We used RNA-seq to analyse the transcriptomic response of Daphnia magna which were fed with two different diets — each with or without supplementation of EPA — at two different temperature levels (15 and 20 °C). The transcripts were mapped to the D. magna genome assembly version 2.4, containing 26,646 translations. When D. magna fed on green alga, changing the temperature provoked a differential expression of 2001 transcripts, and in cyanobacteria-fed daphnia, 3385 transcripts were affected. The supplementation of EPA affected 1635 (on the green algal diet), or 175 transcripts (on the cyanobacterial diet), respectively. Combined effects for diet and temperature were also observed (669 for the green algal and 128 transcripts for the cyanobacterial diet). Searching for orthologous genes (COG-analysis) yielded a functional overview of the altered transcriptomes. Cross-matched transcript sets from both feed types were compiled to illuminate core responses to the factors temperature and EPA-supplementation. Conclusions Our highly controlled eco-physiological experiments revealed an orchestrated response of genes involved in the transformation and signalling of essential fatty acids, including eicosanoid-signalling pathways with potential immune functions. We provide an overview of downstream-regulated genes, which contribute to enhance growth and reproductive output. We also identified numerous EPA-responsive candidate genes of yet unknown function, which constitute new targets for future studies on the molecular basis of EPA-dependent effects at the freshwater plant-herbivore interface.http://link.springer.com/article/10.1186/s12864-019-6268-yOmega-3 fatty acidsEicosapentaenoic acidTemperatureGene expressionDaphnia
collection DOAJ
language English
format Article
sources DOAJ
author Heidrun S. Windisch
Patrick Fink
spellingShingle Heidrun S. Windisch
Patrick Fink
Transcriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipids
BMC Genomics
Omega-3 fatty acids
Eicosapentaenoic acid
Temperature
Gene expression
Daphnia
author_facet Heidrun S. Windisch
Patrick Fink
author_sort Heidrun S. Windisch
title Transcriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipids
title_short Transcriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipids
title_full Transcriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipids
title_fullStr Transcriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipids
title_full_unstemmed Transcriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipids
title_sort transcriptome sequencing of a keystone aquatic herbivore yields insights on the temperature-dependent metabolism of essential lipids
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2019-11-01
description Abstract Background Nutritional quality of phytoplankton is a major determinant of the trophic transfer efficiency at the plant-herbivore interface in freshwater food webs. In particular, the phytoplankton’s content of the essential polyunsaturated omega-3 fatty acid eicosapentaenoic acid (EPA) has been repeatedly shown to limit secondary production in the major zooplankton herbivore genus Daphnia. Despite extensive research efforts on the biological model organism Daphnia, and the availability of several Daphnia genomes, little is known regarding the molecular mechanisms underlying the limitations in Daphnia related to dietary EPA availability. Results We used RNA-seq to analyse the transcriptomic response of Daphnia magna which were fed with two different diets — each with or without supplementation of EPA — at two different temperature levels (15 and 20 °C). The transcripts were mapped to the D. magna genome assembly version 2.4, containing 26,646 translations. When D. magna fed on green alga, changing the temperature provoked a differential expression of 2001 transcripts, and in cyanobacteria-fed daphnia, 3385 transcripts were affected. The supplementation of EPA affected 1635 (on the green algal diet), or 175 transcripts (on the cyanobacterial diet), respectively. Combined effects for diet and temperature were also observed (669 for the green algal and 128 transcripts for the cyanobacterial diet). Searching for orthologous genes (COG-analysis) yielded a functional overview of the altered transcriptomes. Cross-matched transcript sets from both feed types were compiled to illuminate core responses to the factors temperature and EPA-supplementation. Conclusions Our highly controlled eco-physiological experiments revealed an orchestrated response of genes involved in the transformation and signalling of essential fatty acids, including eicosanoid-signalling pathways with potential immune functions. We provide an overview of downstream-regulated genes, which contribute to enhance growth and reproductive output. We also identified numerous EPA-responsive candidate genes of yet unknown function, which constitute new targets for future studies on the molecular basis of EPA-dependent effects at the freshwater plant-herbivore interface.
topic Omega-3 fatty acids
Eicosapentaenoic acid
Temperature
Gene expression
Daphnia
url http://link.springer.com/article/10.1186/s12864-019-6268-y
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