Pronounced Uptake and Metabolism of Organic Substrates by Diatoms Revealed by Pulse-Labeling Metabolomics

Diatoms contribute as a dominant group of microalgae to approximately 20% of the global carbon fixation. In the plankton, these photosynthetic algae are exposed to a plethora of metabolites, especially when competing algae are lysed. It is well established that diatoms can take up specific metabolit...

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Main Authors: Nils Meyer, Aljoscha Rydzyk, Georg Pohnert
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2022.821167/full
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author Nils Meyer
Aljoscha Rydzyk
Georg Pohnert
Georg Pohnert
author_facet Nils Meyer
Aljoscha Rydzyk
Georg Pohnert
Georg Pohnert
author_sort Nils Meyer
collection DOAJ
description Diatoms contribute as a dominant group of microalgae to approximately 20% of the global carbon fixation. In the plankton, these photosynthetic algae are exposed to a plethora of metabolites, especially when competing algae are lysed. It is well established that diatoms can take up specific metabolites, such as vitamins, amino acids as nitrogen source, or dimethylsulfoniopropoionate to compensate for changes in water salinity. It is, however, unclear to which extent diatoms take up other organic resources and if these are incorporated into the cell´s metabolism. Here, we explore the general scope of uptake of metabolites from competitors. Using labeled metabolites released during lysis of algae grown under a 13CO2 atmosphere, we show that the cosmopolitan diatom Chaetoceros didymus takes up even dilute organic substrates from these lysates with little bias for molecular weight or polarity. This is reflected by a high degree of labeling in the metabolome of the exposed cells. The newly developed pulse label/mass spectrometry metabolomics approach reveals that polarity and molecular weight has no detectable influence on uptake. We further show that the taken-up metabolites are partly maintained without metabolic modification within the cells, but also a substantial part is subject to catabolic and anabolic transformation. One of the most dominant phytoplankton groups thus has the potential to compete with heterotrophs, suggesting that the observed osmotrophy may substantially impact organic material fluxes in the oceans. Our findings call for the refinement of our understanding of competition in the plankton.
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spelling doaj.art-32a1dad535214848b4dba3638c0c8d582022-12-22T01:52:48ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-04-01910.3389/fmars.2022.821167821167Pronounced Uptake and Metabolism of Organic Substrates by Diatoms Revealed by Pulse-Labeling MetabolomicsNils Meyer0Aljoscha Rydzyk1Georg Pohnert2Georg Pohnert3Institute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich Schiller University Jena, Jena, GermanyInstitute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich Schiller University Jena, Jena, GermanyInstitute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich Schiller University Jena, Jena, GermanyMax Planck Institute for Chemical Ecology, Jena, GermanyDiatoms contribute as a dominant group of microalgae to approximately 20% of the global carbon fixation. In the plankton, these photosynthetic algae are exposed to a plethora of metabolites, especially when competing algae are lysed. It is well established that diatoms can take up specific metabolites, such as vitamins, amino acids as nitrogen source, or dimethylsulfoniopropoionate to compensate for changes in water salinity. It is, however, unclear to which extent diatoms take up other organic resources and if these are incorporated into the cell´s metabolism. Here, we explore the general scope of uptake of metabolites from competitors. Using labeled metabolites released during lysis of algae grown under a 13CO2 atmosphere, we show that the cosmopolitan diatom Chaetoceros didymus takes up even dilute organic substrates from these lysates with little bias for molecular weight or polarity. This is reflected by a high degree of labeling in the metabolome of the exposed cells. The newly developed pulse label/mass spectrometry metabolomics approach reveals that polarity and molecular weight has no detectable influence on uptake. We further show that the taken-up metabolites are partly maintained without metabolic modification within the cells, but also a substantial part is subject to catabolic and anabolic transformation. One of the most dominant phytoplankton groups thus has the potential to compete with heterotrophs, suggesting that the observed osmotrophy may substantially impact organic material fluxes in the oceans. Our findings call for the refinement of our understanding of competition in the plankton.https://www.frontiersin.org/articles/10.3389/fmars.2022.821167/fullphytoplankton interactionsdiatomsabsorbotrophymixotrophymass spectrometryOsmotrophy
spellingShingle Nils Meyer
Aljoscha Rydzyk
Georg Pohnert
Georg Pohnert
Pronounced Uptake and Metabolism of Organic Substrates by Diatoms Revealed by Pulse-Labeling Metabolomics
Frontiers in Marine Science
phytoplankton interactions
diatoms
absorbotrophy
mixotrophy
mass spectrometry
Osmotrophy
title Pronounced Uptake and Metabolism of Organic Substrates by Diatoms Revealed by Pulse-Labeling Metabolomics
title_full Pronounced Uptake and Metabolism of Organic Substrates by Diatoms Revealed by Pulse-Labeling Metabolomics
title_fullStr Pronounced Uptake and Metabolism of Organic Substrates by Diatoms Revealed by Pulse-Labeling Metabolomics
title_full_unstemmed Pronounced Uptake and Metabolism of Organic Substrates by Diatoms Revealed by Pulse-Labeling Metabolomics
title_short Pronounced Uptake and Metabolism of Organic Substrates by Diatoms Revealed by Pulse-Labeling Metabolomics
title_sort pronounced uptake and metabolism of organic substrates by diatoms revealed by pulse labeling metabolomics
topic phytoplankton interactions
diatoms
absorbotrophy
mixotrophy
mass spectrometry
Osmotrophy
url https://www.frontiersin.org/articles/10.3389/fmars.2022.821167/full
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