Skip to main content

Lund University Publications

LUND UNIVERSITY LIBRARIES

Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms

McQuaid, Jeffrey B. ; Kustka, Adam B. ; Oborník, Miroslav ; Horák, Aleš ; McCrow, John P. ; Karas, Bogumil J. ; Zheng, Hong ; Kindeberg, Theodor LU orcid ; Andersson, Andreas J. and Barbeau, Katherine A. , et al. (2018) In Nature 555(7697). p.534-537
Abstract

In vast areas of the ocean, the scarcity of iron controls the growth and productivity of phytoplankton. Although most dissolved iron in the marine environment is complexed with organic molecules, picomolar amounts of labile inorganic iron species (labile iron) are maintained within the euphotic zone and serve as an important source of iron for eukaryotic phytoplankton and particularly for diatoms. Genome-enabled studies of labile iron utilization by diatoms have previously revealed novel iron-responsive transcripts, including the ferric iron-concentrating protein ISIP2A, but the mechanism behind the acquisition of picomolar labile iron remains unknown. Here we show that ISIP2A is a phytotransferrin that independently and convergently... (More)

In vast areas of the ocean, the scarcity of iron controls the growth and productivity of phytoplankton. Although most dissolved iron in the marine environment is complexed with organic molecules, picomolar amounts of labile inorganic iron species (labile iron) are maintained within the euphotic zone and serve as an important source of iron for eukaryotic phytoplankton and particularly for diatoms. Genome-enabled studies of labile iron utilization by diatoms have previously revealed novel iron-responsive transcripts, including the ferric iron-concentrating protein ISIP2A, but the mechanism behind the acquisition of picomolar labile iron remains unknown. Here we show that ISIP2A is a phytotransferrin that independently and convergently evolved carbonate ion-coordinated ferric iron binding. Deletion of ISIP2A disrupts high-affinity iron uptake in the diatom Phaeodactylum tricornutum, and uptake is restored by complementation with human transferrin. ISIP2A is internalized by endocytosis, and manipulation of the seawater carbonic acid system reveals a second-order dependence on the concentrations of labile iron and carbonate ions. In P. tricornutum, the synergistic interaction of labile iron and carbonate ions occurs at environmentally relevant concentrations, revealing that carbonate availability co-limits iron uptake. Phytotransferrin sequences have a broad taxonomic distribution and are abundant in marine environmental genomic datasets, suggesting that acidification-driven declines in the concentration of seawater carbonate ions will have a negative effect on this globally important eukaryotic iron acquisition mechanism.

(Less)
Please use this url to cite or link to this publication:
author
; ; ; ; ; ; ; ; and , et al. (More)
; ; ; ; ; ; ; ; ; and (Less)
publishing date
type
Contribution to journal
publication status
published
subject
in
Nature
volume
555
issue
7697
pages
4 pages
publisher
Nature Publishing Group
external identifiers
  • scopus:85044265918
  • pmid:29539640
ISSN
0028-0836
DOI
10.1038/nature25982
language
English
LU publication?
no
id
f2d47d14-5310-4294-a3c2-f8cd23e6bc4a
date added to LUP
2019-03-07 14:50:19
date last changed
2024-06-11 06:03:52
@article{f2d47d14-5310-4294-a3c2-f8cd23e6bc4a,
  abstract     = {{<p>In vast areas of the ocean, the scarcity of iron controls the growth and productivity of phytoplankton. Although most dissolved iron in the marine environment is complexed with organic molecules, picomolar amounts of labile inorganic iron species (labile iron) are maintained within the euphotic zone and serve as an important source of iron for eukaryotic phytoplankton and particularly for diatoms. Genome-enabled studies of labile iron utilization by diatoms have previously revealed novel iron-responsive transcripts, including the ferric iron-concentrating protein ISIP2A, but the mechanism behind the acquisition of picomolar labile iron remains unknown. Here we show that ISIP2A is a phytotransferrin that independently and convergently evolved carbonate ion-coordinated ferric iron binding. Deletion of ISIP2A disrupts high-affinity iron uptake in the diatom Phaeodactylum tricornutum, and uptake is restored by complementation with human transferrin. ISIP2A is internalized by endocytosis, and manipulation of the seawater carbonic acid system reveals a second-order dependence on the concentrations of labile iron and carbonate ions. In P. tricornutum, the synergistic interaction of labile iron and carbonate ions occurs at environmentally relevant concentrations, revealing that carbonate availability co-limits iron uptake. Phytotransferrin sequences have a broad taxonomic distribution and are abundant in marine environmental genomic datasets, suggesting that acidification-driven declines in the concentration of seawater carbonate ions will have a negative effect on this globally important eukaryotic iron acquisition mechanism.</p>}},
  author       = {{McQuaid, Jeffrey B. and Kustka, Adam B. and Oborník, Miroslav and Horák, Aleš and McCrow, John P. and Karas, Bogumil J. and Zheng, Hong and Kindeberg, Theodor and Andersson, Andreas J. and Barbeau, Katherine A. and Allen, Andrew E.}},
  issn         = {{0028-0836}},
  language     = {{eng}},
  month        = {{03}},
  number       = {{7697}},
  pages        = {{534--537}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature}},
  title        = {{Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms}},
  url          = {{http://dx.doi.org/10.1038/nature25982}},
  doi          = {{10.1038/nature25982}},
  volume       = {{555}},
  year         = {{2018}},
}