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An H-ferritin from the hydrothermal vent shrimp Rimicaris exoculata and its potential role in iron metabolism

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Abstract

Rimicaris exoculata (Decapoda: Bresiliidae) is one of the dominant species among hydrothermal vent communities along the Mid-Atlantic Ridge. This shrimp can tolerate high concentrations of heavy metals such as iron, but the mechanisms used for detoxification and utilization of excess metals remain largely unknown. Ferritin is a major iron storage protein in most living organisms. The central heavy subunit of ferritin (H-ferritin) possesses ferroxidase activity and converts iron from Fe2+ to Fe3+, the non-toxic form used for storage. In the present study, the H-ferritin RexFrtH was identified in the hydrothermal vent shrimp R. exoculata, and found to be highly expressed in the gill, the main organ involved in bioaccumulation of metals, at both RNA and protein levels. Accumulation of RexFrtH decreased from efferent to afferent vessels, coinciding with the direction of water flow through the gills. Fe3+ was localized with RexFrtH, and in vitro iron-binding and ferroxidase assays using recombinant RexFrtH confirmed the high affinity for iron. Based on these results, we propose a model of iron metabolism in R. exoculata gills; ferrous iron from ambient hydrothermal water accumulates and is converted and stored in ferric form by RexFrtH as an iron reservoir when needed for metabolism, or excreted as an intermediate to prevent iron overload. The findings expand our understanding of the adaptation strategies used by shrimps inhabiting extreme hydrothermal vents to cope with extremely high heavy metal concentrations.

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Acknowledgements

We thank Dr. Zongze Shao and Yingbao Gai [Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, Fujian 361005, PR China] for providing the invaluable samples of Rimicaris exoculata. We also thank Dr. Jingqun Yuan for the assistance with the ICP-MS analysis. This work was supported by the 973 Program of China (Grant Number 2015CB755903); the National Natural Sciences Foundation of China (Grant Numbers 41376133 and 41406175); and the Natural Science Foundation of Zhejiang Province (Grant Numbers LY18C040002 and LQ14H040005).

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Correspondence to Wei-Jun Yang or Jin-Shu Yang.

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Liu, XL., Ye, S., Li, HW. et al. An H-ferritin from the hydrothermal vent shrimp Rimicaris exoculata and its potential role in iron metabolism. Biometals 32, 251–264 (2019). https://doi.org/10.1007/s10534-019-00174-8

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  • DOI: https://doi.org/10.1007/s10534-019-00174-8

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