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BioMetals

, Volume 32, Issue 2, pp 251–264 | Cite as

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

  • Xiao-Li Liu
  • Sen Ye
  • Hua-Wei Li
  • Bo Lu
  • Yan-Qin Yu
  • Yu-Peng Fan
  • Wei-Jun YangEmail author
  • Jin-Shu YangEmail author
Article
  • 122 Downloads

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.

Keywords

H-ferritin Hydrothermal vent Rimicaris exoculata Bioaccumulation Heavy metals Adaptation 

Notes

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).

Compliance with ethical standards

Conflict of interest

The authors declare that there are no competing interests.

Supplementary material

10534_2019_174_MOESM1_ESM.docx (78.2 mb)
Supplementary material 1 (DOCX 80052 kb)

References

  1. Arosio P, Ingrassia R, Cavadini P (2009) Ferritins: a family of molecules for iron storage, antioxidation and more. Biochim Biophys Acta 1790:589–599.  https://doi.org/10.1016/j.bbagen.2008.09.004 CrossRefGoogle Scholar
  2. Arosio P, Carmona F, Gozzelino R, Maccarinelli F, Poli M (2015) The importance of eukaryotic ferritins in iron handling and cytoprotection. Biochem J 472:1–15.  https://doi.org/10.1042/bj20150787 CrossRefGoogle Scholar
  3. 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
  4. Bouabdallah F (2010) The iron redox and hydrolysis chemistry of the ferritins. Biochim Biophys Acta 1800:719–731.  https://doi.org/10.1016/j.bbagen.2010.03.021 CrossRefGoogle Scholar
  5. Bubner B, Baldwin IT (2004) Use of real-time PCR for determining copy number and zygosity in transgenic plants. Plant Cell Rep 23:263–271.  https://doi.org/10.1007/s00299-004-0859-y CrossRefGoogle Scholar
  6. Chevaldonné P, Desbruyères D, Haître ML (1991) Time-series of temperature from three deep-sea hydrothermal vent sites. Deep Sea Res A 38:1417–1430.  https://doi.org/10.1016/0198-0149(91)90014-7 CrossRefGoogle Scholar
  7. Collins TJ (2007) ImageJ for microscopy. Biotechniques 43(1 Suppl):25–30.  https://doi.org/10.2144/000112517 CrossRefGoogle Scholar
  8. Corbari L, Zbinden M, Marie-Anne CB, Gaill F, Compere P (2008) Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata. Aquat Biol 1(3):225–238.  https://doi.org/10.3354/ab00024 CrossRefGoogle Scholar
  9. 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
  10. Distel DL, Lee HK, Cavanaugh CM (1995) Intracellular coexistence of methano- and thioautotrophic bacteria in a hydrothermal vent mussel. Proc Natl Acad Sci USA 92:9598–9602.  https://doi.org/10.1073/pnas.92.21.9598 CrossRefGoogle Scholar
  11. 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
  12. Gebruk AV, Southward EC, Kennedy H, Southward AJ (2000) Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J Marine Biol Assoc United Kingdom 80:485–499CrossRefGoogle Scholar
  13. 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
  14. 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
  15. Guri M, Durand L, Cueffgauchard V, Zbinden M, Crassous P, Shillito B, Bonavita C (2012) Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata. ISME J 6:597.  https://doi.org/10.1038/ismej.2011.133 CrossRefGoogle Scholar
  16. Hügler M, Grtner A, Imhoff JF (2010) Functional genes as markers for sulfur cycling and CO2 fixation in microbial communities of hydrothermal vents of the Logatchev field. FEMS Microbiol Ecol 73:526–537.  https://doi.org/10.1111/j.1574-6941.2010.00919.x Google Scholar
  17. Hügler M, Petersen JM, Dubilier N, Imhoff JF, Sievert SM (2011) Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS ONE 6:e16018.  https://doi.org/10.1371/journal.pone.0016018 CrossRefGoogle Scholar
  18. 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
  19. Khare G, Gupta V, Nangpal P, Gupta RK, Sauter NK, Tyagi A (2011) Ferritin structure from Mycobacterium tuberculosis: comparative study with homologues identifies extended C-terminus involved in ferroxidase activity. PLoS ONE.  https://doi.org/10.1371/journal.pone.0018570 Google Scholar
  20. Kong P, Wang L, Zhang H, Zhou Z, Qiu L, Gai Y, Song L (2010) Two novel secreted ferritins involved in immune defense of Chinese mitten crab Eriocheir sinensis. Fish Shellfish Immunol 28:604–612.  https://doi.org/10.1016/j.fsi.2009.12.018 CrossRefGoogle Scholar
  21. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  22. Kurz T, Eaton JW, Brunk UT (2011) The role of lysosomes in iron metabolism and recycling. Int J Biochem Cell Biol 43:1686–1697.  https://doi.org/10.1016/j.biocel.2011.08.016 CrossRefGoogle Scholar
  23. Lonsdale P (1977) Deep-tow observations at the mounds abyssal hydrothermal field, Galapagos Rift. Earth Planet Sci Lett 36:92–110.  https://doi.org/10.1016/0012-821x(77)90191-1 CrossRefGoogle Scholar
  24. 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
  25. Martinez AS, Charmantier G, Compère P, Charmantier-Daures M (2005) Branchial chamber tissues in two caridean shrimps: the epibenthic Palaemon adspersus, and the deep-sea hydrothermal Rimicaris exoculata. Tissue Cell 37:153–165.  https://doi.org/10.1016/j.tice.2004.12.004 CrossRefGoogle Scholar
  26. Nye V, Copley JT, Tyler PA, Tsikliras AC (2013) Spatial Variation in the Population Structure and Reproductive Biology of Rimicaris hybisae (Caridea: Alvinocarididae) at Hydrothermal Vents on the Mid-Cayman Spreading Centre. PLoS ONE 8(3):e60319CrossRefGoogle Scholar
  27. Pepi S, Sansone L, Chicca M, Marrocchino E, Vaccaro C (2016) Distribution of rare earth elements in soil and grape berries of Vitis vinifera cv. “glera”. Environ Monit Assess. 188:477.  https://doi.org/10.1007/s10661-016-5490-1 CrossRefGoogle Scholar
  28. 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
  29. 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
  30. Qiu GF, Zheng L, Liu P (2008) Transcriptional regulation of ferritin mRNA levels by iron in the freshwater giant prawn, Macrobrachium rosenbergii. Comp Biochem Physiol B 150:320–325.  https://doi.org/10.1016/j.cbpb.2008.03.016 CrossRefGoogle Scholar
  31. Ramirezllodra E, Shank TM, German CR (2007) Biodiversity and biogeography of hydrothermal vent species: thirty years of discovery and investigations. Oceanogr Soc 20:30–41.  https://doi.org/10.5670/oceanog.2007.78 CrossRefGoogle Scholar
  32. Renninger GH, Kass L, Gleeson RA, Van Dover CL, Battelle B-A, Jinks RN, Herzog ED, Chamberlain SC (1995) Sulfide as a Chemical Stimulus for Deep-Sea Hydrothermal Vent Shrimp. Biol Bull 189(2):69–76CrossRefGoogle Scholar
  33. Rosas-Arellano A, Vásquez-Procopio J, Gambis A, Blowes LM, Steller H, Mollereau B, Missirlis F (2016) Ferritin assembly in enterocytes. Int J Mol Sci.  https://doi.org/10.3390/ijms17020027 Google Scholar
  34. Saito MA, Noble AE, Tagliabue A, Goepfert TJ, Lamborg CH, Jenkins WJ (2013) Slow-spreading submarine ridges in the South Atlantic as a significant oceanic iron source. Nat Geosci 6:775–779.  https://doi.org/10.1038/ngeo1893 CrossRefGoogle Scholar
  35. Sarrazin J (1997) Biological and geological dynamics over four years on a high-temperature sulfide structure at the juan de fuca ridge hydrothermal observatory. Mar Ecol Prog Ser 153(1):5–24.  https://doi.org/10.3354/meps153005 CrossRefGoogle Scholar
  36. 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
  37. 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
  38. Tan C, Cino CD, Ding K, Seyfried WE (2017) High temperature hydrothermal vent fluids in Yellowstone lake: observations and insights from in situ pH and redox measurements. J Volcanol Geotherm Res 343:56.  https://doi.org/10.1016/j.jvolgeores.2017.07.017 CrossRefGoogle Scholar
  39. Theil EC (1994) Iron regulatory elements (IREs): a family of mRNA non-coding sequences. Biochem J 304:1.  https://doi.org/10.1042/bj3040001 CrossRefGoogle Scholar
  40. 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
  41. Van Dover CL, Fry B, Grassle JF, Humphris S, Rona PA (1988) Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Mar Biol 98:209–216.  https://doi.org/10.1007/bf00391196 CrossRefGoogle Scholar
  42. Williams AB, Rona PA (1986) Two new caridean shrimps (Bresiliidae) from a hydrothermal field on the Mid-Atlantic Ridge. J Crustac Biol 6:446–462.  https://doi.org/10.1163/193724086x00299 CrossRefGoogle Scholar
  43. Xu J, Shi S, Wang L, Tang Z, Lv T, Zhu X, Ding X, Wang Y, Zhao FJ, Wu Z (2017) Oshac4 is critical for arsenate tolerance and regulates arsenic accumulation in rice. New Phytol 215:1090.  https://doi.org/10.1111/nph.14572 CrossRefGoogle Scholar
  44. Zbinden M, Bris NL, Compere P, Gaill F (2004) Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes. Mar Ecol Prog 284:237–251.  https://doi.org/10.3354/meps284237 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.College of Life SciencesZhejiang UniversityHangzhouPeople’s Republic of China
  2. 2.Key Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Second Institute of OceanographyMinistry of Natural ResourcesHangzhouPeople’s Republic of China
  3. 3.Department of Clinical Laboratory, Women’s HospitalZhejiang University School of MedicineHangzhouPeople’s Republic of China

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