Cobalamin Scarcity Modifies Carbon Allocation and Impairs DMSP Production Through Methionine Metabolism in the Haptophyte Microalgae Tisochrysis lutea

Cobalamin (vitamin B12) is a cobalt-containing enzymatic cofactor involved in methionine synthesis. Provided only by select bacteria and archaea in marine systems, this vitamin is known to limit primary production in different oceanic areas. Understanding the consequences of cobalamin limitation on...

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Main Authors: Charlotte Nef, Céline Henry, Élodie Nicolau, Jean-Baptiste Bérard, Fabienne Hervé, Amandine M. N. Caruana, Raymond Kaas, Francis Mairet, Matthieu Garnier
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmars.2020.569560/full
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author Charlotte Nef
Céline Henry
Élodie Nicolau
Jean-Baptiste Bérard
Fabienne Hervé
Amandine M. N. Caruana
Raymond Kaas
Francis Mairet
Matthieu Garnier
author_facet Charlotte Nef
Céline Henry
Élodie Nicolau
Jean-Baptiste Bérard
Fabienne Hervé
Amandine M. N. Caruana
Raymond Kaas
Francis Mairet
Matthieu Garnier
author_sort Charlotte Nef
collection DOAJ
description Cobalamin (vitamin B12) is a cobalt-containing enzymatic cofactor involved in methionine synthesis. Provided only by select bacteria and archaea in marine systems, this vitamin is known to limit primary production in different oceanic areas. Understanding the consequences of cobalamin limitation on phytoplankton physiology is of great interest, notably for cobalamin-dependent haptophytes that significantly contribute to oceanic carbon fixation and sulfur cycle through dimethyl sulfonio propionate (DMSP) synthesis. Here, the effect of cobalamin limitation was compared to nitrogen limitation on the model haptophyte Tisochrysis lutea grown in chemostats, combining comparative proteomics with the analysis of major macromolecules and specific osmolytes. Our results highlight the interconnection of carbon and DMSP metabolisms through the cobalamin-dependent methionine synthesis by showing that cobalamin scarcity impacts the mechanisms of carbon allocation and reduces DMSP quota. Conversely, proline production seemed to anticorrelate with cobalamin availability. In a boarder context, analysis of transcriptomes or genomes of main DMSP producers from different phytoplankton lineages suggests that most of them are cobalamin-dependent, which means that prokaryotic cobalamin synthesis exerts an important control on phytoplankton DMSP production in some regions of the world ocean.
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spelling doaj.art-b4c4ef96274e40dc959d105a963e66352022-12-22T00:39:21ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452020-10-01710.3389/fmars.2020.569560569560Cobalamin Scarcity Modifies Carbon Allocation and Impairs DMSP Production Through Methionine Metabolism in the Haptophyte Microalgae Tisochrysis luteaCharlotte Nef0Céline Henry1Élodie Nicolau2Jean-Baptiste Bérard3Fabienne Hervé4Amandine M. N. Caruana5Raymond Kaas6Francis Mairet7Matthieu Garnier8IFREMER, Physiology and Biotechnology of Algae Laboratory, Nantes, FrancePAPPSO, Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceIFREMER, Physiology and Biotechnology of Algae Laboratory, Nantes, FranceIFREMER, Physiology and Biotechnology of Algae Laboratory, Nantes, FranceIFREMER, Phycotoxins Laboratory, Nantes, FranceIFREMER, Phycotoxins Laboratory, Nantes, FranceIFREMER, Physiology and Biotechnology of Algae Laboratory, Nantes, FranceIFREMER, Physiology and Biotechnology of Algae Laboratory, Nantes, FranceIFREMER, Physiology and Biotechnology of Algae Laboratory, Nantes, FranceCobalamin (vitamin B12) is a cobalt-containing enzymatic cofactor involved in methionine synthesis. Provided only by select bacteria and archaea in marine systems, this vitamin is known to limit primary production in different oceanic areas. Understanding the consequences of cobalamin limitation on phytoplankton physiology is of great interest, notably for cobalamin-dependent haptophytes that significantly contribute to oceanic carbon fixation and sulfur cycle through dimethyl sulfonio propionate (DMSP) synthesis. Here, the effect of cobalamin limitation was compared to nitrogen limitation on the model haptophyte Tisochrysis lutea grown in chemostats, combining comparative proteomics with the analysis of major macromolecules and specific osmolytes. Our results highlight the interconnection of carbon and DMSP metabolisms through the cobalamin-dependent methionine synthesis by showing that cobalamin scarcity impacts the mechanisms of carbon allocation and reduces DMSP quota. Conversely, proline production seemed to anticorrelate with cobalamin availability. In a boarder context, analysis of transcriptomes or genomes of main DMSP producers from different phytoplankton lineages suggests that most of them are cobalamin-dependent, which means that prokaryotic cobalamin synthesis exerts an important control on phytoplankton DMSP production in some regions of the world ocean.https://www.frontiersin.org/article/10.3389/fmars.2020.569560/fullcobalaminvitamin B12haptophyte microalgaeTisochrysis luteaDMSPchemostat
spellingShingle Charlotte Nef
Céline Henry
Élodie Nicolau
Jean-Baptiste Bérard
Fabienne Hervé
Amandine M. N. Caruana
Raymond Kaas
Francis Mairet
Matthieu Garnier
Cobalamin Scarcity Modifies Carbon Allocation and Impairs DMSP Production Through Methionine Metabolism in the Haptophyte Microalgae Tisochrysis lutea
Frontiers in Marine Science
cobalamin
vitamin B12
haptophyte microalgae
Tisochrysis lutea
DMSP
chemostat
title Cobalamin Scarcity Modifies Carbon Allocation and Impairs DMSP Production Through Methionine Metabolism in the Haptophyte Microalgae Tisochrysis lutea
title_full Cobalamin Scarcity Modifies Carbon Allocation and Impairs DMSP Production Through Methionine Metabolism in the Haptophyte Microalgae Tisochrysis lutea
title_fullStr Cobalamin Scarcity Modifies Carbon Allocation and Impairs DMSP Production Through Methionine Metabolism in the Haptophyte Microalgae Tisochrysis lutea
title_full_unstemmed Cobalamin Scarcity Modifies Carbon Allocation and Impairs DMSP Production Through Methionine Metabolism in the Haptophyte Microalgae Tisochrysis lutea
title_short Cobalamin Scarcity Modifies Carbon Allocation and Impairs DMSP Production Through Methionine Metabolism in the Haptophyte Microalgae Tisochrysis lutea
title_sort cobalamin scarcity modifies carbon allocation and impairs dmsp production through methionine metabolism in the haptophyte microalgae tisochrysis lutea
topic cobalamin
vitamin B12
haptophyte microalgae
Tisochrysis lutea
DMSP
chemostat
url https://www.frontiersin.org/article/10.3389/fmars.2020.569560/full
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