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

Research output: Contribution to journalArticle

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 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.

Details

Authors
  • Jeffrey B. McQuaid
  • Adam B. Kustka
  • Miroslav Oborník
  • Aleš Horák
  • John P. McCrow
  • Bogumil J. Karas
  • Hong Zheng
  • Theodor Kindeberg
  • Andreas J. Andersson
  • Katherine A. Barbeau
  • Andrew E. Allen
External organisations
  • J. Craig Venter Institute, San Diego
  • University of California, San Diego
  • Rutgers University-Newark Campus
  • Institute of Parasitology, Czech Academy of Sciences
  • University of South Bohemia
Research areas and keywords

Subject classification (UKÄ) – MANDATORY

  • Ecology
Original languageEnglish
Pages (from-to)534-537
Number of pages4
JournalNature
Volume555
Issue number7697
Publication statusPublished - 2018 Mar 22
Publication categoryResearch
Peer-reviewedYes
Externally publishedYes