An H-ferritin from the hydrothermal vent shrimp Rimicaris exoculata and its potential role in iron metabolism
- 122 Downloads
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.
KeywordsH-ferritin Hydrothermal vent Rimicaris exoculata Bioaccumulation Heavy metals Adaptation
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).
Compliance with ethical standards
Conflict of interest
The authors declare that there are no competing interests.
- Beedessee G, Watanabe H, Ogura T, Nemoto S, Yahagi T, Nakagawa S, Nakamura K, Takai K, Koonjul M, Marie DEP (2013) High connectivity of animal populations in deep-sea hydrothermal vent fields in the Central Indian Ridge relevant to its geological setting. PLoS ONE 8:e81570. https://doi.org/10.1371/journal.pone.0081570 CrossRefGoogle Scholar
- Cottin D, Shillito B, Chertemps T, Thatje S, Léger N, Ravaux J (2010) Comparison of heat-shock responses between the hydrothermal vent shrimp Rimicaris exoculata, and the related coastal shrimp Palaemonetes varians. J Exp Mar Biol Ecol 393:9–16. https://doi.org/10.1016/j.jembe.2010.06.008 CrossRefGoogle Scholar
- Douville E, Charlou JL, Oelkers EH, Bienvenu P, Colon CFJ, Donval JP, Fouquet Y, Prieur D, Appriou P (2002) The rainbow vent fluids (36°14′N, MAR): the influence of ultramafic rocks and phase separation on trace metal content in Mid-Atlantic Ridge hydrothermal fluids. Chem Geol 184:37–48. https://doi.org/10.1016/s0009-2541(01)00351-5 CrossRefGoogle Scholar
- Geret F, Riso R, Sarradin PM, Caprais JC, Cosson R (2002) Metal bioaccumulation and storage forms in the shrimp, Rimicaris exoculata, from the rainbow hydrothermal field (Mid-Atlantic Ridge); preliminary approach to the fluid-organism relationship. Cah Biol Mar 43:45–52. https://doi.org/10.21411/CBM.A.C6A03AC Google Scholar
- Gollner S, Kaiser S, Menzel L, Jones D, Brown A, Mestre NC, Oevelen D, Menot L, Colaco A, Canals M, Cuvelier D, Durden JM, Gebruk A, Egho GA, Haeckel M, Marcon Y, Mevenkamp L, Morato T, Arbizu PM (2017) Resilience of benthic deep-sea fauna to mining activities. Mar Environ Res 129:76. https://doi.org/10.1016/j.marenvres.2017.04.010 CrossRefGoogle Scholar
- Jan C, Petersen JM, Werner J, Teeling H, Huang S, Glöckner FO, Golyshina OV, Dubilier N, Golyshin PN, Jebbar M, Bonavita C (2014) The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: an in-depth metagenomic investigation and discovery of Zetaproteobacteria. Environ Microbiol 16:2723–2738. https://doi.org/10.1111/1462-2920.12406 CrossRefGoogle Scholar
- M’Kandawire E, Mierekadamska A, Stürzenbaum SR, Choongo K, Yabe J, Mwase M, Saasa N, Blindauer CA (2017) Metallothionein from wild populations of the African catfish Clarias gariepinus: from sequence, protein expression and metal binding properties to transcriptional biomarker of metal pollution. Int J Mol Sci 18:1548. https://doi.org/10.3390/ijms18071548 CrossRefGoogle Scholar
- Petersen JM, Ramette A, Lott C, Cambon-Bonavita MA, Zbinden M, Dubilier N (2010) Dual symbiosis of the vent shrimp Rimicaris exoculata, with filamentous Gamma- and Epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environ Microbiol 12:2204–2218. https://doi.org/10.1111/j.1462-2920.2009.02129.x Google Scholar
- Ponsard J, Cambon-Bonavita M-A, Zbinden M, Lepoint G, Joassin A, Corbari L, Shillito B, Durand L, Cueff-Gauchard V, Compère P (2013) Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata. ISME J 7(1):96–109CrossRefGoogle Scholar
- Schmidt C, Bris NL, Gaill F (2008) Interactions of deep-sea vent invertebrates with their environment: the case of Rimicaris exoculata. J Shellfish Res 27:79–90. https://doi.org/10.2983/0730-8000(2008)27%5b79:IODVIW%5d2.0.CO;2 CrossRefGoogle Scholar
- Shibuya T, Yoshizaki M, Masaki Y, Suzuki K, Takai K, Russell MJ (2013) Reactions between basalt and CO2-rich seawater at 250 and 350 °C, 500 bars: implications for the CO2, sequestration into the modern oceanic crust and the composition of hydrothermal vent fluid in the CO2-rich early ocean. Chem Geol 359(3):1–9. https://doi.org/10.1016/j.chemgeo.2013.08.044 CrossRefGoogle Scholar
- Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994:4673–4680. https://doi.org/10.1007/978-1-4020-6754-9_3188 CrossRefGoogle Scholar