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Short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts

In large areas of the ocean, iron concentrations are insufficient to promote phytoplankton growth. Numerous studies have been conducted to characterize the effect of iron on algae and how algae cope with fluctuating iron concentrations. Fertilization experiments in low-iron areas resulted primarily...

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Autores principales: Behnke, Joerg, Cai, Yun, Gu, Hong, LaRoche, Julie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9873189/
https://www.ncbi.nlm.nih.gov/pubmed/36693065
http://dx.doi.org/10.1371/journal.pone.0280827
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author Behnke, Joerg
Cai, Yun
Gu, Hong
LaRoche, Julie
author_facet Behnke, Joerg
Cai, Yun
Gu, Hong
LaRoche, Julie
author_sort Behnke, Joerg
collection PubMed
description In large areas of the ocean, iron concentrations are insufficient to promote phytoplankton growth. Numerous studies have been conducted to characterize the effect of iron on algae and how algae cope with fluctuating iron concentrations. Fertilization experiments in low-iron areas resulted primarily in diatom-dominated algal blooms, leading to laboratory studies on diatoms comparing low- and high-iron conditions. Here, we focus on the short-term temporal response following iron addition to an iron-starved open ocean diatom, Thalassiosira oceanica. We employed the NanoString platform and analyzed a high-resolution time series on 54 transcripts encoding proteins involved in photosynthesis, N-linked glycosylation, iron transport, as well as transcription factors. Nine transcripts were iron-responsive, with an immediate response to the addition of iron. The fastest response observed was the decrease in transcript levels of proteins involved in iron uptake, followed by an increase in transcript levels of iron-containing enzymes and a simultaneous decrease in the transcript levels of their iron-free replacement enzymes. The transcription inhibitor actinomycin D was used to understand the underlying mechanisms of the decrease of the iron-responsive transcripts and to determine their half-lives. Here, Mn-superoxide dismutase (Mn-SOD), plastocyanin (PETE), ferredoxin (PETF) and cellular repressor of EA1-stimulated genes (CREGx2) revealed longer than average half-lives. Four iron-responsive transcripts showed statistically significant differences in their decay rates between the iron-recovery samples and the actD treatment. These differences suggest regulatory mechanisms influencing gene transcription and mRNA stability. Overall, our study contributes towards a detailed understanding of diatom cell biology in the context of iron fertilization response and provides important observations to assess oceanic diatom responses following sudden changes in iron concentrations.
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spelling pubmed-98731892023-01-25 Short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts Behnke, Joerg Cai, Yun Gu, Hong LaRoche, Julie PLoS One Research Article In large areas of the ocean, iron concentrations are insufficient to promote phytoplankton growth. Numerous studies have been conducted to characterize the effect of iron on algae and how algae cope with fluctuating iron concentrations. Fertilization experiments in low-iron areas resulted primarily in diatom-dominated algal blooms, leading to laboratory studies on diatoms comparing low- and high-iron conditions. Here, we focus on the short-term temporal response following iron addition to an iron-starved open ocean diatom, Thalassiosira oceanica. We employed the NanoString platform and analyzed a high-resolution time series on 54 transcripts encoding proteins involved in photosynthesis, N-linked glycosylation, iron transport, as well as transcription factors. Nine transcripts were iron-responsive, with an immediate response to the addition of iron. The fastest response observed was the decrease in transcript levels of proteins involved in iron uptake, followed by an increase in transcript levels of iron-containing enzymes and a simultaneous decrease in the transcript levels of their iron-free replacement enzymes. The transcription inhibitor actinomycin D was used to understand the underlying mechanisms of the decrease of the iron-responsive transcripts and to determine their half-lives. Here, Mn-superoxide dismutase (Mn-SOD), plastocyanin (PETE), ferredoxin (PETF) and cellular repressor of EA1-stimulated genes (CREGx2) revealed longer than average half-lives. Four iron-responsive transcripts showed statistically significant differences in their decay rates between the iron-recovery samples and the actD treatment. These differences suggest regulatory mechanisms influencing gene transcription and mRNA stability. Overall, our study contributes towards a detailed understanding of diatom cell biology in the context of iron fertilization response and provides important observations to assess oceanic diatom responses following sudden changes in iron concentrations. Public Library of Science 2023-01-24 /pmc/articles/PMC9873189/ /pubmed/36693065 http://dx.doi.org/10.1371/journal.pone.0280827 Text en © 2023 Behnke et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Behnke, Joerg
Cai, Yun
Gu, Hong
LaRoche, Julie
Short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts
title Short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts
title_full Short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts
title_fullStr Short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts
title_full_unstemmed Short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts
title_short Short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts
title_sort short-term response to iron resupply in an iron-limited open ocean diatom reveals rapid decay of iron-responsive transcripts
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9873189/
https://www.ncbi.nlm.nih.gov/pubmed/36693065
http://dx.doi.org/10.1371/journal.pone.0280827
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