Complex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability

ABSTRACT The productivity of the ocean is largely dependent on iron availability, and marine phytoplankton have evolved sophisticated mechanisms to cope with chronically low iron levels in vast regions of the open ocean. By analyzing the metabarcoding data generated from the Tara Oceans expedition,...

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Autores principales:	Eva Kotabova, Ronald Malych, Juan José Pierella Karlusich, Elena Kazamia, Meri Eichner, Jan Mach, Emmanuel Lesuisse, Chris Bowler, Ondřej Prášil, Robert Sutak
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Bigelowiella natans iron metagenomics metatranscriptomics photosynthesis phytoplankton Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f52b56350c2c4cadba0494c29d01889b
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spelling	oai:doaj.org-article:f52b56350c2c4cadba0494c29d01889b2021-12-02T18:20:19ZComplex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability10.1128/mSystems.00738-202379-5077https://doaj.org/article/f52b56350c2c4cadba0494c29d01889b2021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00738-20https://doaj.org/toc/2379-5077ABSTRACT The productivity of the ocean is largely dependent on iron availability, and marine phytoplankton have evolved sophisticated mechanisms to cope with chronically low iron levels in vast regions of the open ocean. By analyzing the metabarcoding data generated from the Tara Oceans expedition, we determined how the global distribution of the model marine chlorarachniophyte Bigelowiella natans varies across regions with different iron concentrations. We performed a comprehensive proteomics analysis of the molecular mechanisms underpinning the adaptation of B. natans to iron scarcity and report on the temporal response of cells to iron enrichment. Our results highlight the role of phytotransferrin in iron homeostasis and indicate the involvement of CREG1 protein in the response to iron availability. Analysis of the Tara Oceans metagenomes and metatranscriptomes also points to a similar role for CREG1, which is found to be widely distributed among marine plankton but to show a strong bias in gene and transcript abundance toward iron-deficient regions. Our analyses allowed us to define a new subfamily of the CobW domain-containing COG0523 putative metal chaperones which are involved in iron metabolism and are restricted to only a few phytoplankton lineages in addition to B. natans. At the physiological level, we elucidated the mechanisms allowing a fast recovery of PSII photochemistry after resupply of iron. Collectively, our study demonstrates that B. natans is well adapted to dynamically respond to a changing iron environment and suggests that CREG1 and COG0523 are important components of iron homeostasis in B. natans and other phytoplankton. IMPORTANCE Despite low iron availability in the ocean, marine phytoplankton require considerable amounts of iron for their growth and proliferation. While there is a constantly growing knowledge of iron uptake and its role in the cellular processes of the most abundant marine photosynthetic groups, there are still largely overlooked branches of the eukaryotic tree of life, such as the chlorarachniophytes. In the present work, we focused on the model chlorarachniophyte Bigelowiella natans, integrating physiological and proteomic analyses in culture conditions with the mining of omics data generated by the Tara Oceans expedition. We provide unique insight into the complex responses of B. natans to iron availability, including novel links to iron metabolism conserved in other phytoplankton lineages.Eva KotabovaRonald MalychJuan José Pierella KarlusichElena KazamiaMeri EichnerJan MachEmmanuel LesuisseChris BowlerOndřej PrášilRobert SutakAmerican Society for MicrobiologyarticleBigelowiella natansironmetagenomicsmetatranscriptomicsphotosynthesisphytoplanktonMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bigelowiella natans iron metagenomics metatranscriptomics photosynthesis phytoplankton Microbiology QR1-502
spellingShingle	Bigelowiella natans iron metagenomics metatranscriptomics photosynthesis phytoplankton Microbiology QR1-502 Eva Kotabova Ronald Malych Juan José Pierella Karlusich Elena Kazamia Meri Eichner Jan Mach Emmanuel Lesuisse Chris Bowler Ondřej Prášil Robert Sutak Complex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability
description	ABSTRACT The productivity of the ocean is largely dependent on iron availability, and marine phytoplankton have evolved sophisticated mechanisms to cope with chronically low iron levels in vast regions of the open ocean. By analyzing the metabarcoding data generated from the Tara Oceans expedition, we determined how the global distribution of the model marine chlorarachniophyte Bigelowiella natans varies across regions with different iron concentrations. We performed a comprehensive proteomics analysis of the molecular mechanisms underpinning the adaptation of B. natans to iron scarcity and report on the temporal response of cells to iron enrichment. Our results highlight the role of phytotransferrin in iron homeostasis and indicate the involvement of CREG1 protein in the response to iron availability. Analysis of the Tara Oceans metagenomes and metatranscriptomes also points to a similar role for CREG1, which is found to be widely distributed among marine plankton but to show a strong bias in gene and transcript abundance toward iron-deficient regions. Our analyses allowed us to define a new subfamily of the CobW domain-containing COG0523 putative metal chaperones which are involved in iron metabolism and are restricted to only a few phytoplankton lineages in addition to B. natans. At the physiological level, we elucidated the mechanisms allowing a fast recovery of PSII photochemistry after resupply of iron. Collectively, our study demonstrates that B. natans is well adapted to dynamically respond to a changing iron environment and suggests that CREG1 and COG0523 are important components of iron homeostasis in B. natans and other phytoplankton. IMPORTANCE Despite low iron availability in the ocean, marine phytoplankton require considerable amounts of iron for their growth and proliferation. While there is a constantly growing knowledge of iron uptake and its role in the cellular processes of the most abundant marine photosynthetic groups, there are still largely overlooked branches of the eukaryotic tree of life, such as the chlorarachniophytes. In the present work, we focused on the model chlorarachniophyte Bigelowiella natans, integrating physiological and proteomic analyses in culture conditions with the mining of omics data generated by the Tara Oceans expedition. We provide unique insight into the complex responses of B. natans to iron availability, including novel links to iron metabolism conserved in other phytoplankton lineages.
format	article
author	Eva Kotabova Ronald Malych Juan José Pierella Karlusich Elena Kazamia Meri Eichner Jan Mach Emmanuel Lesuisse Chris Bowler Ondřej Prášil Robert Sutak
author_facet	Eva Kotabova Ronald Malych Juan José Pierella Karlusich Elena Kazamia Meri Eichner Jan Mach Emmanuel Lesuisse Chris Bowler Ondřej Prášil Robert Sutak
author_sort	Eva Kotabova
title	Complex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability
title_short	Complex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability
title_full	Complex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability
title_fullStr	Complex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability
title_full_unstemmed	Complex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability
title_sort	complex response of the chlorarachniophyte <named-content content-type="genus-species">bigelowiella natans</named-content> to iron availability
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/f52b56350c2c4cadba0494c29d01889b
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Complex Response of the Chlorarachniophyte <named-content content-type="genus-species">Bigelowiella natans</named-content> to Iron Availability

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