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

Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms
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DOI:
10.1038/nature25982
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发表时间:
2018-03-22
期刊:
影响因子:
64.8
通讯作者:
Allen, Andrew E.
Allen, Andrew E.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
McQuaid, Jeffrey B.;Kustka, Adam B.;Allen, Andrew E.

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在海洋的广大地区,铁的缺乏控制着浮游植物的生长和生产力(1,2)。尽管海洋环境中的大多数溶解铁与有机分子络合(3),但皮摩尔量的不稳定无机铁物种(不稳定铁)保持在真光层(4)内,并作为真核浮游植物,特别是硅藻的重要铁来源(5)。硅藻对不稳定铁的利用的基因组研究先前已经揭示了新的铁响应转录物(6,7),包括三价铁浓缩蛋白ISIP2A(8),但获得皮摩尔不稳定铁的机制仍然未知。在这里,我们表明,ISIP2A是一种植物转铁蛋白,独立和收敛地发展碳酸根离子协调三价铁结合。ISIP2A的缺失破坏了硅藻三角褐指藻的高亲和力铁吸收,并通过与人转铁蛋白互补恢复了吸收。ISIP2A是内化的内吞作用,海水碳酸系统的操纵揭示了不稳定的铁和碳酸根离子的浓度的二阶依赖性。在三角褐指藻中,不稳定铁和碳酸根离子的协同相互作用发生在环境相关浓度下,表明碳酸根的可用性共同限制铁的吸收。植物转铁蛋白序列具有广泛的分类学分布(8),并且在海洋环境基因组数据集中丰富(9,10),这表明酸化驱动的海水碳酸根离子浓度下降将对这种全球重要的真核生物铁获取机制产生负面影响。
In vast areas of the ocean, the scarcity of iron controls the growth and productivity of phytoplankton(1,2). Although most dissolved iron in the marine environment is complexed with organic molecules(3), picomolar amounts of labile inorganic iron species (labile iron) are maintained within the euphotic zone(4) and serve as an important source of iron for eukaryotic phytoplankton and particularly for diatoms(5). Genome-enabled studies of labile iron utilization by diatoms have previously revealed novel iron responsive transcripts(6,7), including the ferric iron-concentrating protein ISIP2A(8), 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(8) and are abundant in marine environmental genomic datasets(9,10), 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.