|Title||Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms|
|Publication Type||Journal Article|
|Year of Publication||2018|
|Authors||McQuaid JB, Kustka AB, Oborník M, Horák A, McCrow JP, Karas BJ, Zheng H, Kindeberg T, Andersson AJ, Barbeau KA, Allen AE|
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.
The requirement for synergistic binding reveals the existence of a previously undescribed form of iron–carbonate co-limitation29 that may be relevant in environments in which primary productivity is limited by [Fe]. Like transferrin, phytotransferrin exploits carbonate chemistry to function as both coordination anion and internalization release trigger13, resulting in a mechanism that is exquisitely sensitive to acidification-induced changes in [CO32−]. Our results show that under constant [Fe′], the doubling of CO2 to 800 p.p.m. CO2 can reduce P. tricornutum Fe′ uptake rates by 44%. While Fe′ is an important component of phytoplankton nutrition5, we also show that P. tricornutum can use phytotransferrin-independent pathways to access organically complexed iron. In the marine environment, this pool of complexed iron is much larger3, although uptake rates can be orders of magnitude slower30, underscoring the trade-off inherent to the different iron acquisition strategies. As iron-limited regions exert an important influence on global biogeochemical cycles1, we view these results as a starting point for understanding the complex and interdependent influences of ocean acidification on phytoplankton iron uptake mechanisms and rates