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Sources and Forms of Trace Metals Taken Up by Hydrothermal Vent Mussels, and Possible Adaption and Mitigation Strategies

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Part of the book series: The Handbook of Environmental Chemistry ((HEC,volume 50))

Abstract

Vent mussels are ubiquitous in most hydrothermal fields, despite the metal-rich environment they live in, with dissolved metal ions, colloidal and particulate metal forms in concentrations orders of magnitude higher than in ambient seawater. Different studies at various hydrothermally active sites on the Mid-Atlantic Ridge and East Pacific Rise have shown that metal concentrations in the tissues of the mussel generally reflect metal loads of their environments, displaying spatial gradients, with bioconcentration factors up to 105. Gills and digestive glands accumulate the highest amounts of metals, which is related to their direct role in food uptake, while mantle and foot show moderate metal enrichments. Metal uptake in the form of mineral particles has been identified as an important source of metals in the mussel tissues. While closer to the active vent sites metal sulfides forming during mixing of hot hydrothermal fluid and seawater are more dominant, with increasing distance iron oxides with metals adsorbed from seawater play a more important role for metal accumulation by the vent mussels. Although the shells of hydrothermal mussels have low metal concentrations compared to the soft tissues, they are a record of the chemical composition of the seawater – hydrothermal fluid mixture. Different species of Bathymodiolus mussels from the Pacific and Atlantic display similar metal accumulations and adaptation strategies, while vent clams show some similarities, but also some differences compared to Bathymodiolus.

Some of the metals (e.g., alkali and earth alkaline elements, Zn and Mn) taken up by the mussels appear to be bioregulated. They are essential elements and their concentration ranges in the mussel tissues are usually less variable than other heavy metals, although their variability in the fluids is comparably high. Strategies of the vent mussels to cope with high concentrations of potentially toxic metals such as Cu, Cd, and Hg include binding to metallothioneins, which are strongly metal-binding proteins, and possibly immobilization of the metals in the form of granules stored in the tissue. These ways of mitigating heavy metal toxicity have also been found for other organisms including non-vent bivalves. Another yet to be proven possibility is the excretion of organic ligands into the water which binds to the metals and makes them less bioavailable.

Due to the challenges of sampling hydrothermal vent mussels and their environmental compartments, many questions remain open or hypotheses still need to be tested; studies often differ in their approach and a comparison of results is not straightforward. Hence, more systematic studies focusing on specific metal groups, experiments under defined conditions and a comparison of different species of vent mussels are desirable. Apart from the many open questions that refer directly to the understanding of metal accumulation and adaptation of hydrothermal vent mussels to their challenging environment, a better knowledge in this field may also help to support other fields of research. These include estimation of hydrothermal metal fluxes into the ocean and elucidation of survival strategies of organisms in other metal-rich environments.

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References

  1. Tunnicliff V (1991) The biology of hydrothermal vents: ecology and evolution. Oceanogr Mar Biol Annu Rev 29:319–407

    Google Scholar 

  2. Page HM, Fiala-Medioni A, Fisher CR, Childress JJ (1991) Experimental evidence for filter-feeding by the hydrothermal vent mussel, Bathymodiolus thermophilus. Deep Sea Res A Oceanogr Res Pap 38:1455–1461. doi:10.1016/0198-0149(91)90084-S

    Article  Google Scholar 

  3. Fiala-Médioni A, McKiness Z, Dando P, Boulegue J, Mariotti A, Alayse-Danet A, Robinson J, Cavanaugh C (2002) Ultrastructural, biochemical, and immunological characterization of two populations of the mytilid mussel Bathymodiolus azoricus from the Mid-Atlantic Ridge: evidence for a dual symbiosis. Mar Biol 141:1035–1043

    Article  Google Scholar 

  4. Fiala-Médioni A, Michalski JC, Jollès J, Alonso C, Montreuil J (1994) Lysosomic and lysozyme activities in the gill of bivalves from deep hydrothermal vents. C R Acad Sci III Sci Vie 317:239–244

    Google Scholar 

  5. Perner M, Bach W, Hentscher M, Koschinsky A, Garbe-Schönberg D, Streit WR, Strauss H (2009) Short-term microbial and physico-chemical variability in low-temperature hydrothermal fluids near 5°S on the Mid-Atlantic Ridge. Environ Microbiol 11:2526–2541

    Article  CAS  Google Scholar 

  6. Martins I, Cosson RP, Riou V, Sarradin P, Sarrazin J, Santos RS, Colaço A (2011) Relationship between metal levels in the vent mussel Bathymodiolus azoricus and local microhabitat chemical characteristics of Eiffel Tower (Lucky Strike). Deep Sea Res I Oceanogr Res Pap 58:306–315

    Article  CAS  Google Scholar 

  7. Johnson KS, Childress JJ, Beehler CL, Sakamoto CM (1994) Biogeochemistry of hydrothermal vent mussel communities: the deep-sea analogue to the intertidal zone. Deep Sea Res I Oceanogr Res Pap 41:993–1011. doi:10.1016/0967-0637(94)90015-9

    Article  CAS  Google Scholar 

  8. Nedoncelle K, Lartaud F, Contreira Pereira L, Yücel M, Thurnherr AM, Mullineaux L, Le Bris N (2015) Bathymodiolus growth dynamics in relation to environmental fluctuations in vent habitats. Deep Sea Res I Oceanogr Res Pap 106:183–193

    Article  Google Scholar 

  9. Mottl MJ, McConachy TF (1990) Chemical processes in buoyant hydrothermal plumes on the East Pacific Rise near 21°N. Geochim Cosmochim Acta 54:1911–1927

    Article  CAS  Google Scholar 

  10. James R, Parks G (1982) Characterization of aqueous colloids by their electrical double-layer and intrinsic surface chemical properties. In: Matijević E (ed) Surface and colloid science. Springer, New York, pp 119–216

    Chapter  Google Scholar 

  11. Sunda WG, Ferguson RL (1983) Sensitivity of natural bacterial communities to additions of copper and to cupric ion activity: a bioassay of copper complexation in seawater. In: Trace metals in seawater, vol 9. Plenum Press, New York, pp 871–891

    Chapter  Google Scholar 

  12. Sarradin P, Waeles M, Bernagout S, Le Gall C, Sarrazin J, Riso R (2009) Speciation of dissolved copper within an active hydrothermal edifice on the Lucky Strike vent field (MAR, 37°N). Sci Total Environ 407:869–878

    Article  CAS  Google Scholar 

  13. Johnson KS, Childress JJ, Beehler CL (1988) Short-term temperature variability in the Rose Garden hydrothermal vent field: an unstable deep-sea environment. Deep Sea Res A Oceanogr Res Pap 35:1711–1721

    Article  Google Scholar 

  14. Edgcomb VP, Molyneaux SJ, Saito MA, Lloyd K, Böer S, Wirsen CO, Atkins MS, Teske A (2004) Sulfide ameliorates metal toxicity for deep-sea hydrothermal vent archaea. Appl Environ Microbiol 70:2551–2555

    Article  CAS  Google Scholar 

  15. Trevisan R, Ferraz Mello D, Fisher AS, Schuwerack P, Dafre AL, Moody AJ (2011) Selenium in water enhances antioxidant defenses and protects against copper-induced DNA damage in the blue mussel Mytilus edulis. Aquat Toxicol 101:64–71

    Article  CAS  Google Scholar 

  16. Wang W, Rainbow PS (2005) Influence of metal exposure history on trace metal uptake and accumulation by marine invertebrates. Ecotoxicol Environ Saf 61:145–159

    Article  CAS  Google Scholar 

  17. Eisler R (1981) Trace metal concentrations in marine organisms. Pergamon Press, Oxford, p 685

    Google Scholar 

  18. Martins I, Colaço A, Dando PR, Martins I, Desbruyères D, Sarradin P, Marques JC, Serrão-Santos R (2008) Size-dependent variations on the nutritional pathway of Bathymodiolus azoricus demonstrated by a C-flux model. Ecol Model 217:59–71

    Article  Google Scholar 

  19. Demina LL, Holm NG, Galkin SV, Lein AY (2013) Some features of the trace metal biogeochemistry in the deep-sea hydrothermal vent fields (Menez Gwen, Rainbow, Broken Spur at the MAR and 9°50′N at the EPR): a synthesis. J Mar Syst 126:94–105

    Article  Google Scholar 

  20. Koschinsky A, Kausch M, Borowski C (2014) Metal concentrations in the tissues of the hydrothermal vent mussel Bathymodiolus: reflection of different metal sources. Mar Environ Res 95:62–73

    Article  CAS  Google Scholar 

  21. Cosson RP, Thiébaut É, Company R, Castrec-Rouelle M, Colaço A, Martins I, Sarradin P, Bebianno MJ (2008) Spatial variation of metal bioaccumulation in the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 65:405–415

    Article  CAS  Google Scholar 

  22. Martins I, Costa V, Porteiro F, Cravo A, Santos RS (2001) Mercury concentrations in invertebrates from Mid-Atlantic Ridge hydrothermal vent fields. J Mar Biol Assoc U K 81:913–915

    Article  CAS  Google Scholar 

  23. Smith DR, Flegal AR (1989) Elemental concentrations of hydrothermal vent organisms from the Galápagos Rift. Mar Biol 102:127–133

    Article  CAS  Google Scholar 

  24. Dubilier N, Windoffer R, Giere O (1998) Ultrastructure and stable carbon isotope composition of the hydrothermal vent mussels’ Bathymodiolus brevior and B. sp. affinis brevior from the North Fiji Basin, western Pacific. Mar Ecol Prog Ser 165:187–193

    Article  Google Scholar 

  25. Demina LL, Galkin SV (2008) On the role of abiogenic factors in the bioaccumulation of heavy metals by the hydrothermal fauna of the Mid-Atlantic Ridge. Oceanology 48:784–797

    Article  Google Scholar 

  26. Jeffree RA, Markich SJ, Brown PL (1993) Comparative accumulation of alkaline-earth metals by two freshwater mussel species from the Nepean River, Australia: consistences and a resolved paradox. Mar Freshw Res 44:609–634

    Article  CAS  Google Scholar 

  27. Bara M, Guiet-Bara A, Durlach J (1993) Regulation of sodium and potassium pathways by magnesium in cell membranes. Magnes Res 6:167–177

    CAS  Google Scholar 

  28. Von Damm KL (1995) Controls on the chemistry and temporal variability of seafloor hydrothermal fluids. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds) Seafloor hydrothermal systems: physical, chemical, biological, and geological interactions. American Geophysical Union, Washington, DC, pp 222–247

    Chapter  Google Scholar 

  29. Colaço A, Bustamante P, Fouquet Y, Sarradin PM, Serrão-Santos R (2006) Bioaccumulation of Hg, Cu, and Zn in the Azores triple junction hydrothermal vent fields food web. Chemosphere 65:2260–2267

    Article  Google Scholar 

  30. Kádár E, Costa V, Segonzac M (2007) Trophic influences of metal accumulation in natural pollution laboratories at deep-sea hydrothermal vents of the Mid-Atlantic Ridge. Sci Total Environ 373:464–472

    Article  Google Scholar 

  31. Lee S, Kim S, Ju S, Pak S, Son S, Yang J, Han S (2015) Mercury accumulation in hydrothermal vent mollusks from the southern Tonga Arc, southwestern Pacific Ocean. Chemosphere 127:246–253

    Article  CAS  Google Scholar 

  32. Taylor VF, Jackson BP, Siegfried M, Navratilova J, Francesconi KA, Kirshtein J, Voytek M (2012) Arsenic speciation in food chains from Mid-Atlantic hydrothermal vents. Environ Chem 9:130–138

    Article  CAS  Google Scholar 

  33. Rousse N, Boulegue J, Cosson RP, Fiala-Medioni A (1998) Bioaccumulation des métaux chez le mytilidae hydrothermal Bathymodiolus sp. de la ride médio-atlantique. Oceanol Acta 21:597–607

    Article  CAS  Google Scholar 

  34. Geret F, Rousse N, Riso R, Sarradin P, Coson RP (1998) Metal compartmentalization and metallothionein isoforms in mussels form the Mid-Atlantic Ridge; preliminary approach to the fluid–organism relationship. Cah Biol Mar 39:291–293

    Google Scholar 

  35. Roesijadi G, Crecelius EA (1984) Elemental composition of the hydrothermal vent clam Calyptogena magnifica from the East Pacific Rise. Mar Biol 83:155–161

    Article  CAS  Google Scholar 

  36. Roesijadi G, Young JS, Crecelius EA, Thomas LE (1985) Distribution of trace metals in the hydrothermal vent clam, Calyptogena magnifica. Bull Biol Soc Wash 6:311–324

    Google Scholar 

  37. Ruelas-Inzunza J, Soto LA, Páez-Osuna F (2003) Heavy-metal accumulation in the hydrothermal vent clam Vesicomya gigas from Guaymas basin, Gulf of California. Deep Sea Res I Oceanogr Res Pap 50:757–761

    Article  CAS  Google Scholar 

  38. Kádár E, Santos RS, Powell JJ (2006) Biological factors influencing tissue compartmentalization of trace metals in the deep-sea hydrothermal vent bivalve Bathymodiolus azoricus at geochemically distinct vent sites of the Mid-Atlantic Ridge. Environ Res 101:221–229

    Article  Google Scholar 

  39. Kádár E, Costa V, Santos RS, Powell JJ (2006) Tissue partitioning of micro-essential metals in the vent bivalve Bathymodiolus azoricus and associated organisms (endosymbiont bacteria and a parasite polychaete) from geochemically distinct vents of the Mid-Atlantic Ridge. J Sea Res 56:45–52

    Article  Google Scholar 

  40. Charmasson S, Le Faouder A, Loyen J, Cosson RP, Sarradin P (2011) 210Po and 210Pb in the tissues of the deep-sea hydrothermal vent mussel Bathymodiolus azoricus from the Menez Gwen field (Mid-Atlantic Ridge). Sci Total Environ 409:771–777

    Article  CAS  Google Scholar 

  41. Kádár E, Costa V (2006) First report on the micro-essential metal concentrations in bivalve shells from deep-sea hydrothermal vents. J Sea Res 56:37–44

    Article  Google Scholar 

  42. Bau M, Balan S, Schmidt K, Koschinsky A (2010) Rare earth elements in mussel shells of the Mytilidae family as tracers for hidden and fossil high-temperature hydrothermal systems. Earth Planet Sci Lett 299:310–316

    Article  CAS  Google Scholar 

  43. Ponnurangam A, Bau M, Brenner M, Koschinsky A (2016) Mussel shells of Mytilus edulis as bioarchives of the distribution of rare earth elements and yttrium in seawater and the potential impact of pH and temperature on their partitioning behavior. Biogeosciences 13:751–760

    Article  Google Scholar 

  44. Klerks PL, Fraleigh PC (1997) Uptake of nickel and zinc by the zebra mussel Dreissena polymorpha. Arch Environ Contam Toxicol 32:191–197

    Article  CAS  Google Scholar 

  45. Bellotto VR, Miekeley N (2007) Trace metals in mussel shells and corresponding soft tissue samples: a validation experiment for the use of Perna perna shells in pollution monitoring. Anal Bioanal Chem 389:769–776

    Article  CAS  Google Scholar 

  46. Deplede MH, Rainbow PS (1990) Models of regulation and accumulation of trace metals in marine invertebrates. Comp Biochem Physiol 97C:1–7

    Google Scholar 

  47. Hardivillier Y, Leignel V, Denis F, Uguen G, Cosson R, Laulier M (2004) Do organisms living around hydrothermal vent sites contain specific metallothioneins? The case of the genus Bathymodiolus (Bivalvia, Mytilidae). Comp Biochem Physiol C Toxicol Pharmacol 139:111–118

    Article  Google Scholar 

  48. Company R, Serafim A, Cosson RP, Fiala-Médioni A, Camus L, Serrão-Santos R, João Bebianno M (2010) Sub-lethal effects of cadmium on the antioxidant defence system of the hydrothermal vent mussel Bathymodiolus azoricus. Ecotoxicol Environ Saf 73:788–795

    Article  CAS  Google Scholar 

  49. Gonzales-Rey M, Serafim A, Company R, Gomes T, Bebianno MM (2008) Detoxification mechanisms in shrimp: comparative approach between hydrothermal vent fields and estuarine environments. Mar Environ Res 66:35–37

    Article  Google Scholar 

  50. Klevenz V, Sander SG, Perner M, Koschinsky A (2012) Amelioration of free copper by hydrothermal vent microbes as a response to high copper concentrations. Chem Ecol 28:405–420

    Article  CAS  Google Scholar 

  51. Marigomez I, Soto M, Cajaraville MP, Angulo E, Giamberini L (2002) Cellular and subcellular distribution of metals in molluscs. Microsc Res Tech 56:358–392

    Article  CAS  Google Scholar 

  52. Giere O, Borowski C (2001) Chapter 7: Bakterien-Tier-Symbiosen als Charakteristika hydrothermaler Ökosysteme. In: Hydrothermale Fluidentwicklung, Stoffbilanzierung und spezielle biologische Aktivität im Nord-Fidschi-Becken - HYFIFLUX II - SO 134" - In German unpublished. Abschlussbericht (Final report BMBF project Project) No. 03 G 0134:154

    Google Scholar 

  53. Bryan GW (1984) Pollution due to heavy metals and their compounds. In: Kinne O (ed) Marine ecology, 5th edn. Wiley, London, pp 1289–1431

    Google Scholar 

  54. Yücel M, Gartman A, Chan CS, Luther GW III (2011) Hydrothermal vents as a kinetically stable source of iron-sulphide-bearing nanoparticles to the ocean. Nat Geosci 4:367–371

    Article  Google Scholar 

  55. Sander SG, Koschinsky A (2011) Metal flux from hydrothermal vents increased by organic complexation. Nat Geosci 4:145–150

    Article  CAS  Google Scholar 

  56. Larsen EH, Quétel CR, Munoz R, Fiala-Medioni A, Donard OFX (1997) Arsenic speciation in shrimp and mussel from the Mid-Atlantic hydrothermal vents. Mar Chem 57:341–346

    Article  CAS  Google Scholar 

  57. Demina LL, Galkin SV, Shumilin E (2009) Bioaccumulation of some trace elements in the biota of the hydrothermal fields of the Guaymas Basin (Gulf of California). Bol Soc Geol Mex 61:31

    Google Scholar 

  58. Balan AS (2010) Trace metals in the nacreous layer of Mytilidae mussel shells from the North Sea and the Mid Atlantic Ridge as proxies for environmental conditions

    Google Scholar 

  59. Cravo A, Foster P, Almeida C, Bebianno MJ, Company R (2008) Metal concentrations in the shell of Bathymodiolus azoricus from contrasting hydrothermal vent fields on the mid-Atlantic ridge. Mar Environ Res 65:338–348

    Article  CAS  Google Scholar 

  60. Cravo A, Foster P, Almeida C, Company R, Cosson RP, Bebianno MJ (2007) Metals in the shell of Bathymodiolus azoricus from a hydrothermal vent site on the Mid-Atlantic Ridge. Environ Int 33:609–615

    Article  CAS  Google Scholar 

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Acknowledgements

Discussions with Christian Borowski (MPI for Marine Microbiology, Bremen) on biological topics of hydrothermal fauna were very helpful for writing this chapter. Autun Purser (Alfred Wegener Institute for Polar and Marine Research, Bremerhaven) is acknowledged for the drawings in this chapter. A special thanks goes to Adilah Ponnurangam (Jacobs University Bremen) for her general support at various stages of this chapter.

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Koschinsky, A. (2016). Sources and Forms of Trace Metals Taken Up by Hydrothermal Vent Mussels, and Possible Adaption and Mitigation Strategies. In: Demina, L., Galkin, S. (eds) Trace Metal Biogeochemistry and Ecology of Deep-Sea Hydrothermal Vent Systems. The Handbook of Environmental Chemistry, vol 50. Springer, Cham. https://doi.org/10.1007/698_2016_2

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