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

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 l...

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Veröffentlicht in:Biometals 2019-04, Vol.32 (2), p.251-264
Hauptverfasser: Liu, Xiao-Li, Ye, Sen, Li, Hua-Wei, Lu, Bo, Yu, Yan-Qin, Fan, Yu-Peng, Yang, Wei-Jun, Yang, Jin-Shu
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container_issue 2
container_start_page 251
container_title Biometals
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creator Liu, Xiao-Li
Ye, Sen
Li, Hua-Wei
Lu, Bo
Yu, Yan-Qin
Fan, Yu-Peng
Yang, Wei-Jun
Yang, Jin-Shu
description 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 Fe 2+ to Fe 3+ , 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. Fe 3+ 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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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 Fe 2+ to Fe 3+ , 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. Fe 3+ 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.</description><identifier>ISSN: 0966-0844</identifier><identifier>EISSN: 1572-8773</identifier><identifier>DOI: 10.1007/s10534-019-00174-8</identifier><identifier>PMID: 30756217</identifier><language>eng</language><publisher>Dordrecht: Springer Netherlands</publisher><subject>Bioaccumulation ; Biochemistry ; Biomedical and Life Sciences ; Cell Biology ; Decapoda ; Detoxification ; Dominant species ; Ferritin ; Ferroxidase ; Gills ; Heavy metals ; Hydrothermal plumes ; Hydrothermal vents ; Iron ; Life Sciences ; Medicine/Public Health ; Metabolism ; Metal concentrations ; Metals ; Microbiology ; Pharmacology/Toxicology ; Plant Physiology ; Proteins ; Ribonucleic acid ; RNA ; Sensory neurons ; Shrimps ; Vents ; Water flow</subject><ispartof>Biometals, 2019-04, Vol.32 (2), p.251-264</ispartof><rights>Springer Nature B.V. 2019</rights><rights>BioMetals is a copyright of Springer, (2019). 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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 Fe 2+ to Fe 3+ , 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. Fe 3+ 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. 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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 Fe 2+ to Fe 3+ , 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. Fe 3+ 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.</abstract><cop>Dordrecht</cop><pub>Springer Netherlands</pub><pmid>30756217</pmid><doi>10.1007/s10534-019-00174-8</doi><tpages>14</tpages></addata></record>
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subjects Bioaccumulation
Biochemistry
Biomedical and Life Sciences
Cell Biology
Decapoda
Detoxification
Dominant species
Ferritin
Ferroxidase
Gills
Heavy metals
Hydrothermal plumes
Hydrothermal vents
Iron
Life Sciences
Medicine/Public Health
Metabolism
Metal concentrations
Metals
Microbiology
Pharmacology/Toxicology
Plant Physiology
Proteins
Ribonucleic acid
RNA
Sensory neurons
Shrimps
Vents
Water flow
title An H-ferritin from the hydrothermal vent shrimp Rimicaris exoculata and its potential role in iron metabolism
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