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Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis

BACKGROUND: Global change will affect patterns of nutrient upwelling in marine environments, potentially becoming even stricter regulators of phytoplankton primary productivity. To better understand phytoplankton nutrient utilization on the subcellular basis, we assessed the transcriptomic responses...

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Autores principales: Rokitta, Sebastian D, Von Dassow, Peter, Rost, Björn, John, Uwe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4301891/
https://www.ncbi.nlm.nih.gov/pubmed/25467008
http://dx.doi.org/10.1186/1471-2164-15-1051
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author Rokitta, Sebastian D
Von Dassow, Peter
Rost, Björn
John, Uwe
author_facet Rokitta, Sebastian D
Von Dassow, Peter
Rost, Björn
John, Uwe
author_sort Rokitta, Sebastian D
collection PubMed
description BACKGROUND: Global change will affect patterns of nutrient upwelling in marine environments, potentially becoming even stricter regulators of phytoplankton primary productivity. To better understand phytoplankton nutrient utilization on the subcellular basis, we assessed the transcriptomic responses of the life-cycle stages of the biogeochemically important microalgae Emiliania huxleyi to nitrogen-limitation. Cells grown in batch cultures were harvested at ‘early’ and ‘full’ nitrogen-limitation and were compared with non-limited cells. We applied microarray-based transcriptome profilings, covering ~10.000 known E. huxleyi gene models, and screened for expression patterns that indicate the subcellular responses. RESULTS: The diploid life-cycle stage scavenges nitrogen from external organic sources and -like diatoms- uses the ornithine-urea cycle to rapidly turn over cellular nitrogen. The haploid stage reacts similarly, although nitrogen scavenging is less pronounced and lipid oxidation is more prominent. Generally, polyamines and proline appear to constitute major organic pools that back up cellular nitrogen. Both stages induce a malate:quinone-oxidoreductase that efficiently feeds electrons into the respiratory chain and drives ATP generation with reduced respiratory carbon throughput. CONCLUSIONS: The use of the ornithine-urea cycle to budget the cellular nitrogen in situations of limitation resembles the responses observed earlier in diatoms. This suggests that underlying biochemical mechanisms are conserved among distant clades of marine phototrophic protists. The ornithine-urea cycle and proline oxidation appear to constitute a sensory-regulatory system that monitors and controls cellular nitrogen budgets under limitation. The similarity between the responses of the life-cycle stages, despite the usage of different genes, also indicates a strong functional consistency in the responses to nitrogen-limitation that appears to be owed to biochemical requirements. The malate:quinone-oxidoreductase is a genomic feature that appears to be absent from diatom genomes, and it is likely to strongly contribute to the uniquely high endurance of E. huxleyi under nutrient limitation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1051) contains supplementary material, which is available to authorized users.
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spelling pubmed-43018912015-01-22 Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis Rokitta, Sebastian D Von Dassow, Peter Rost, Björn John, Uwe BMC Genomics Research Article BACKGROUND: Global change will affect patterns of nutrient upwelling in marine environments, potentially becoming even stricter regulators of phytoplankton primary productivity. To better understand phytoplankton nutrient utilization on the subcellular basis, we assessed the transcriptomic responses of the life-cycle stages of the biogeochemically important microalgae Emiliania huxleyi to nitrogen-limitation. Cells grown in batch cultures were harvested at ‘early’ and ‘full’ nitrogen-limitation and were compared with non-limited cells. We applied microarray-based transcriptome profilings, covering ~10.000 known E. huxleyi gene models, and screened for expression patterns that indicate the subcellular responses. RESULTS: The diploid life-cycle stage scavenges nitrogen from external organic sources and -like diatoms- uses the ornithine-urea cycle to rapidly turn over cellular nitrogen. The haploid stage reacts similarly, although nitrogen scavenging is less pronounced and lipid oxidation is more prominent. Generally, polyamines and proline appear to constitute major organic pools that back up cellular nitrogen. Both stages induce a malate:quinone-oxidoreductase that efficiently feeds electrons into the respiratory chain and drives ATP generation with reduced respiratory carbon throughput. CONCLUSIONS: The use of the ornithine-urea cycle to budget the cellular nitrogen in situations of limitation resembles the responses observed earlier in diatoms. This suggests that underlying biochemical mechanisms are conserved among distant clades of marine phototrophic protists. The ornithine-urea cycle and proline oxidation appear to constitute a sensory-regulatory system that monitors and controls cellular nitrogen budgets under limitation. The similarity between the responses of the life-cycle stages, despite the usage of different genes, also indicates a strong functional consistency in the responses to nitrogen-limitation that appears to be owed to biochemical requirements. The malate:quinone-oxidoreductase is a genomic feature that appears to be absent from diatom genomes, and it is likely to strongly contribute to the uniquely high endurance of E. huxleyi under nutrient limitation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1051) contains supplementary material, which is available to authorized users. BioMed Central 2014-12-02 /pmc/articles/PMC4301891/ /pubmed/25467008 http://dx.doi.org/10.1186/1471-2164-15-1051 Text en © Rokitta et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Rokitta, Sebastian D
Von Dassow, Peter
Rost, Björn
John, Uwe
Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis
title Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis
title_full Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis
title_fullStr Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis
title_full_unstemmed Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis
title_short Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis
title_sort emiliania huxleyi endures n-limitation with an efficient metabolic budgeting and effective atp synthesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4301891/
https://www.ncbi.nlm.nih.gov/pubmed/25467008
http://dx.doi.org/10.1186/1471-2164-15-1051
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