Vanadium pp 73-92 | Cite as

Hyper-Accumulation of Vanadium in Polychaetes

Chapter

Abstract

The present chapter summarizes our current knowledge on vanadium accumulation in polychaetes, with special emphasis on tube-dwelling fan worms of the Sabellidae family. Some of these species exhibit the unusual capability to hyperaccumulate vanadium at levels several order of magnitude higher than those commonly found in most aquatic organisms. Concentrations higher than 5,000 and 10,000 μg/g were measured in branchial crowns of Pseudopotamilla occelata and Perkinsiana littoralis respectively, stored in vacuoles of the epithelial cells. These tissues appear as feather-like filaments, typically expanded for filter-feeding and respiration activities, while the rest of the body remain protected inside the tube. Feeding trials suggested that the elevated levels of vanadium in branchial filaments of sabellids can act as chemical deterrents against predation in more exposed tissues. A similar function, recently proposed also for the elevated levels of arsenic in branchial crowns of Sabella spallanzanii suggest that hyperaccumulation of toxic metals is a common antipredatory strategy for branchial crowns of sabellid polychaetes, which often results unpalatable for consumers.

Keywords

Vanadium Marine organisms Polychaetes Sabellidae Branchial crowns Hyper-accumulation Subcellular distribution Biological functions Chemical defenses Anti-predatory strategy 

References

  1. 1.
    Butler A (1998) Acquisition and utilization of transition metal ions by marine organisms. Science 281:207–209CrossRefGoogle Scholar
  2. 2.
    Rehder D (2003) Biological and medicinal aspects of vanadium. Inorg Chem Commun 6: 604–617CrossRefGoogle Scholar
  3. 3.
    Sepe A, Ciaralli L, Ciprotti M, Giordano R, Funari E, Costantini S (2003) Determination of cadmium, chromium, lead and vanadium in six fish species from the Adriatic Sea. Food Addit Contam 20:543–552CrossRefGoogle Scholar
  4. 4.
    Trefry JH, Metz S (1989) Role of hydrothermal precipitates in the geochemical cycling of vanadium. Nature 342:531–533CrossRefGoogle Scholar
  5. 5.
    Popham JD, D’Auria JM (1982) A new sentinel organism for vanadium and titanium. Mar Pollut Bull 13:25–27CrossRefGoogle Scholar
  6. 6.
    Ishii T, Otake T, Okoshi K, Nakahara M, Nakamura R (1994) Intracellular localization of vanadium in the fan worm Pseudopotamilla occelata. Mar Biol 121:143–151CrossRefGoogle Scholar
  7. 7.
    Fattorini D, Notti A, Nigro M, Regoli F (2010) Hyperaccumulation of vanadium in the Antarctic polychaete Perkinsiana littoralis as a natural chemical defense against predation. Environ Sci Pollut Res Int 17:220–228CrossRefGoogle Scholar
  8. 8.
    Gibbs PE, Bryan GW, Ryan KP (1981) Copper accumulation by the polychaete Melinna palmata: an antipredation mechanism? J Mar Biol Assoc UK 61:707–722CrossRefGoogle Scholar
  9. 9.
    Fattorini D, Notti A, Halt MN, Gambi MC, Regoli F (2005) Levels and chemical speciation of arsenic in polychaetes: a review. Mar Ecol 26:255–264CrossRefGoogle Scholar
  10. 10.
    Sandrini JZ, Regoli F, Fattorini D, Notti A, Ferreira Inácio A, Linde-Arias AR, Laurino J, Bainy ACS, Marins LFF, Monserrat JM (2006) Short-term responses to cadmium exposure in the estuarine polychaete Laeonereis acuta (polychaeta, Nereididae): subcellular distribution and oxidative stress generation. Environ Toxicol Chem 25:1337–1344CrossRefGoogle Scholar
  11. 11.
    Fukushima M, Suzuki H, Saito K, Chatt A (2008) Vanadium levels in marine organisms of Onagawa Bay in Japan. Environ Monit Assess 141:329–337CrossRefGoogle Scholar
  12. 12.
    Grotti M, Soggia F, Lagomarsino C, Dalla Riva S, Goessler W, Francesconi KA (2008) Natural variability and distribution of trace elements in marine organisms from Antarctic coastal environments. Antarctic Sci 20:39–51CrossRefGoogle Scholar
  13. 13.
    Bellante A, Sprovieri M, Buscaino G, Salvagio Manta D, Buffa G, Di Stefano V, Bonanno A, Barra M, Patti B, Giacoma C, Mazzola S (2009) Trace elements and vanadium in tissues and organs of species of cetaceans from Italian coasts. Chem Ecol 25:311–323CrossRefGoogle Scholar
  14. 14.
    Bashirpoor M, Schmidt H, Schulzke C, Rehder D (1997) Models for vanadate-dependent haloperoxidases: vanadium complexes with 04N-Donor Sets. Chem Ber 130:651–657CrossRefGoogle Scholar
  15. 15.
    Kawakami N, Ueki T, Amata Y, Kanamori K, Matsuo K, Gekko K, Michibata H (2009) A novel vanadium reductase, Vanabin2, forms a possible cascade involved in electron transfer. Biochim Biophys Acta 1794:674–679Google Scholar
  16. 16.
    Michibata H, Hirata J, Uesaka M, Numakunai T, Sakurai H (1987) Separation of vanadocytes: determination and characterization of vanadium ion in the separated blood cells of the ascidian, Ascidia ahodori. J Exp Zool 244:33–38CrossRefGoogle Scholar
  17. 17.
    Michibata H, Hirose H, Sugiyama K, Ookubo Y, Kanamori K (1990) Extraction of a vanadium-binding substance (vanadobin) from the blood cells of several ascidian species. Biol Bull Mar Biol Lab Woods Hole 179:140–147CrossRefGoogle Scholar
  18. 18.
    Michibata H, Terada T, Anada N, Yamakawa K, Numakunai T (1986) The accumulation and distribution of vanadium, iron and manganese in some solitary ascidians. Biol Bull Mar Biol Lab Woods Hole 171:672–681CrossRefGoogle Scholar
  19. 19.
    Michibata H, Uyama T (1990) Extraction of vanadium-binding substances (vanadobin) from a subpopulation of signet ring cells newly identified as vanadocytes in ascidians. J Exp Zool 254:132–137CrossRefGoogle Scholar
  20. 20.
    Michibata H, Uyama T, Ueki T, Kanamori K (2002) Vanadocytes, cells hold the key to resolving the highly selective accumulation and reduction of vanadium in ascidians. Microsc Res Tech 56:421–434CrossRefGoogle Scholar
  21. 21.
    Kanda T, Nose Y, Wuchiyama J, Uyama T, Moriyama Y, Michibata H (1997) Identification of a vanadium-associated protein from the vanadium-rich ascidian, Ascidia sydneiensis samea. Zool Sci 14:37–42CrossRefGoogle Scholar
  22. 22.
    Ueki T, Adachi T, Kawano S, Aoshima M, Yamaguchi N, Kanamori K, Michibata H (2003) Vanadium-binding proteins (vanabins) from a vanadium-rich ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1626:43–50Google Scholar
  23. 23.
    Minganti V, Capelli R, De Pellegrini R (1998) The concentrations of Pb, Cd, Cu, Zn, and V in Adamussium colbecki from Terra Nova Bay (Antarctica). Int J Environ Anal Chem 71: 257–263CrossRefGoogle Scholar
  24. 24.
    El-Naggar MEE, Al-Amoudi OA (1989) Heavy metal levels in several species of marine algae from the Red Sea of Saudi Arabia. JKAU Sci 1:5–13CrossRefGoogle Scholar
  25. 25.
    Lavilla I, Vilas P, Bendicho C (2008) Fast determination of arsenic, selenium, nickel and vanadium in fish and shellfish by electrothermal atomic absorption spectrometry following ultrasound-assisted extraction. Food Chem 106:403–409CrossRefGoogle Scholar
  26. 26.
    Protasowicki M, Dural M, Jaremek J (2008) Trace metals in the shells of blue mussels (Mytilus edulis) from the Poland coast of Baltic sea. Environ Monit Assess 141:329–337CrossRefGoogle Scholar
  27. 27.
    Chiffoleau JF, Chauvaud L, Amouroux D, Barats A, Dufour A (2004) Nickel and vanadium contamination of benthic invertebrates following the “Erika” wreck. Aquat Living Resour 17:273–280CrossRefGoogle Scholar
  28. 28.
    Alfonso JA, Azócar JA, LaBrecque JJ, Benzo Z, Marcano E, Gómez CV, Quintal M (2005) Temporal and spatial variation of trace metals in clams Tivela mactroidea along the Venezuelan coast. Mar Pollut Bull 50:1713–1744CrossRefGoogle Scholar
  29. 29.
    Fattorini D, Notti A, Di Mento R, Cicero AM, Gabellini M, Russo A, Regoli F (2008) Seasonal, spatial and inter-annual variations of trace metals in mussels from the Adriatic Sea: a regional gradient for arsenic and implications for monitoring the impact of off-shore activities. Chemosphere 72:1524–1533CrossRefGoogle Scholar
  30. 30.
    Regoli F (1998) Trace metals and antioxidant enzymes in gills and digestive gland of the Mediterranean mussel Mytilus galloprovincialis. Arch Environ Contam Toxicol 34:48–63CrossRefGoogle Scholar
  31. 31.
    Miramand P, Guary JC (1980) High concentrations of some heavy metals in tissues of the Mediterranean Octopus. Bull Environ Contam Toxicol 24:738–788CrossRefGoogle Scholar
  32. 32.
    Miramand P, Bentley D (1992) Concentration and distribution of heavy metals in tissues of two cephalopods, Eledone cirrhosa and Sepia officinalis, from the French coast of the English Channel. Mar Biol 114:407–414CrossRefGoogle Scholar
  33. 33.
    Miramand P, Bustamante P, Bentley D, Kouéta N (2006) Variation of heavy metal concentrations (Ag, Cd, Co, Cu, Fe, Pb, V and Zn) during the life cycle of the common cuttlefish Sepia officinalis. Sci Total Environ 361:132–143CrossRefGoogle Scholar
  34. 34.
    Bustamante P, Grigioni S, Boucher-Rodoni R, Caurant F, Miramand P (2000) Bioaccumulation of 12 trace elements in the tissues of the nautilus Nautilus macromphalus from New Caledonia. Mar Pollut Bull 40:688–696CrossRefGoogle Scholar
  35. 35.
    Abdel-Moati MAR, Nasir NA (1997) Bioaccumulation of chromium, nickel, lead and vanadium in some commercial fish and prawn from Qatari waters. Qatar Univ Sci J 17:195–203Google Scholar
  36. 36.
    Bu-Olayan AH, Subrahmanyam MNV (1998) Trace metal concentrations in the crab Macrophthalmus depressus and sediments on the Kuwait coast. Environ Monit Assess 53:297–304CrossRefGoogle Scholar
  37. 37.
    Campbell LM, Norstrom RJ, Hobson KA, Muir DCG, Backus S, Fisk AT (2005) Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci Total Environ 351:247–263CrossRefGoogle Scholar
  38. 38.
    Ikemoto T, Tu NPC, Okuda N, Iwata A, Omori K, Tanabe S, Tuyen BC, Takeuchi I (2008) Biomagnification of trace elements in the aquatic food web in the Mekong Delta, South Vietnam using stable carbon and nitrogen isotope analysis. Arch Environ Contam Toxicol 54:504–515CrossRefGoogle Scholar
  39. 39.
    Anan Y, Kunito K, Tanabe S, Mitrofanov I, Aubrey DG (2005) Trace element accumulation in fishes collected from coastal waters of the Caspian Sea. Mar Pollut Bull 51:882–888CrossRefGoogle Scholar
  40. 40.
    Mackey EA, Becker PR, Demiralp R, Greenberg RR, Koster BJ, Wise SA (1996) Bioccumulation of vanadium and other trace metals in liver of Alaskan cetaceans and pinnipeds. Arch Environ Contam Toxicol 30:503–512CrossRefGoogle Scholar
  41. 41.
    Mackey EA, Demiralp R, Becker PR, Greenberg RR, Koster BJ, Wise SA (1995) Trace element concentrations in cetacean liver tissues archived in the National Marine Mammal Tissue Bank. Sci Total Environ 175:25–41CrossRefGoogle Scholar
  42. 42.
    Kunito T, Nakamura S, Ikemoto T, Anan Y, Kubota R, Tanabe S, Rosas CW, Fillmann G, Readman JW (2004) Concentration and subcellular distribution of trace elements in liver of small cetaceans incidentally caught along the Brazilian coast. Mar Pollut Bull 49:574–587CrossRefGoogle Scholar
  43. 43.
    Agusa T, Nomura K, Kunito T, Anan Y, Iwata H, Miyazaki N, Tatsukawa R, Tanabe S (2008) Interelement relationship and age-related variation of trace element concentrations in liver of striped dolphins (Stenella coeruleoalba) from Japanese coastal waters. Mar Pollut Bull 57: 807–815CrossRefGoogle Scholar
  44. 44.
    Young JS, Adee RR, Piscopo I, Buschbom RL (1981) Effects of copper on the sabellid polychaete. Eudistylia vancouveri. II. Copper accumulation and tissue injury in the branchial crown. Arch Environ Contam Toxicol 10:87–104CrossRefGoogle Scholar
  45. 45.
    Young JS, Buschbom RL, Gurtisen JM, Joyce SP (1979) Effects of copper on the sabellid polychaete. Eudistylia vancouveri: I. Concentration limits for copper accumulation. Arch Environ Contam Toxicol 8:97–106CrossRefGoogle Scholar
  46. 46.
    Ishii T, Nakai I, Numako C, Okoshi K, Otake T (1993) Discovery of a new vanadium accumulator, the fan worm Pseudopotamilla occelata. Naturwissenschaften 80:268–270CrossRefGoogle Scholar
  47. 47.
    Bagaveeva EV, Zvyagintsev AY (2000) The introduction of polychaetes Hydroides elegans (Haswell), Polydora limicola (Annenkova), and Pseudopotamilla occelata (Moore) to the Northwestern part of the East Sea. Ocean Res 22:25–36Google Scholar
  48. 48.
    Cole AG, Hall BK (2004) The nature and significance of invertebrate cartilages revisited: distribution and histology of cartilage and cartilage-like tissues within the Metazoa. Zoology 107:261–273CrossRefGoogle Scholar
  49. 49.
    Yoshihara M, Ueki T, Yamaguchi N, Kamino K, Michibata H (2008) Characterization of a novel vanadium-binding protein (VBP-129) from blood plasma of vanadium-rich ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1780:256–263Google Scholar
  50. 50.
    Uyama T, Nose Y, Wuchiyama J, Moriyama Y, Michibata H (1997) Finding of the same antigens in the polychaete, Pseudopotamilla occelata, as those in the vanadium-rich ascidian, Ascidia sydneiensis samea. Zool Sci 14:43–47CrossRefGoogle Scholar
  51. 51.
    Giangrande A, Gambi MC (1997) The genus Perkinsiana (Polychaeta, Sabellidae) from Antarctica, with descriptions of the new species P. milae and P. borsibrunoi. Zool Scripta 26:267–278CrossRefGoogle Scholar
  52. 52.
    Bocchetti R, Fattorini D, Gambi MC, Regoli F (2004) Trace metal concentrations and susceptibility to oxidative stress in the polychaete Sabella spallanzanii (Gmelin) (Sabellidae): potential role of antioxidants in revealing stressful environmental conditions in the Mediterranean. Arch Environ Contam Toxicol 46:353–361CrossRefGoogle Scholar
  53. 53.
    Fattorini D, Bocchetti R, Bompadre S, Regoli F (2004) Total content and chemical speciation of arsenic in the polychaete Sabella spallanzanii. Mar Environ Res 58:839–843CrossRefGoogle Scholar
  54. 54.
    Fattorini D, Regoli F (2004) Arsenic speciation in tissues of the Mediterranean polychaete Sabella spallanzanii. Environ Toxicol Chem 23:1881–1887CrossRefGoogle Scholar
  55. 55.
    Bargagli R (2005) Antarctic ecosystems. Environmental contamination, climate change and human impact. Springer, BerlinGoogle Scholar
  56. 56.
    Lichtenegger HC, Schöberl T, Bartl MH, Waite H, Stucky GD (2002) High abrasion resistance with sparse mineralization: copper biomineral in worm jaws. Science 298:389–392CrossRefGoogle Scholar
  57. 57.
    Lichtenegger HC, Schöberl T, Ruokolainen JT, Cross JO, Heald SM, Birkedal H, Waite JH, Stucky GD (2003) Zinc and mechanical prowess in the jaws of Nereis, a marine worm. P Natl Acad Sci USA 100:9144–9149CrossRefGoogle Scholar
  58. 58.
    Nejmeddine A, Dhainaut-Courtois N, Baert JL, Sautière P, Fournet B, Boulenguer P (1988) Purification and characterization of a cadmium-binding protein from Nereis diversicolor (Annelida, Polychaeta). Comp Biochem Physiol C 89:321–326CrossRefGoogle Scholar
  59. 59.
    McClintock JB, Baker BJ (1997) A review of the chemical ecology of Antarctic marine invertebrates. Am Zool 37:329–342Google Scholar
  60. 60.
    McClintock JB, Baker BJ (2001) Marine chemical ecology, Marine science series. CRC, Boca RatonCrossRefGoogle Scholar
  61. 61.
    Paul VJ, Puglisi MP, Ritson-Williams R (2006) Marine chemical ecology. Nat Prod Res 23:153–180CrossRefGoogle Scholar
  62. 62.
    Kicklighter CE, Hay ME (2006) Integrating prey defensive traits: contrasts of marine worms from temperate and tropical habitats. Ecol Monogr 76:195–215CrossRefGoogle Scholar
  63. 63.
    Kicklighter CE, Hay ME (2007) To avoid or deter: interactions among defensive and escape strategies in sabellid worms. Oecologia 151:161–173CrossRefGoogle Scholar
  64. 64.
    Fattorini D, Alonso-Hernandez CM, Diaz-Asencio M, Munoz-Caravaca A, Pannacciulli FG, Tangherlini M, Regoli F (2004) Chemical speciation of arsenic in different marine organisms: importance in monitoring studies. Mar Environ Res 58:845–850CrossRefGoogle Scholar
  65. 65.
    Fattorini D, Notti A, Regoli F (2006) Characterization of arsenic content in marine organisms from temperate, tropical, and polar environments. Chem Ecol 22:405–414CrossRefGoogle Scholar
  66. 66.
    Ventura-Lima J, Fattorini D, Notti A, Monserrat JM, Regoli F (2010) Bioaccumulation patterns and biological effects of arsenic in aquatic organisms. In: Gosselin JD, Fancher IM (eds) Environmental health risks: lead poisoning and arsenic exposure. Nova Science Publishers Inc., New York, Chapter 6. ISBN 978-1-60741-781-1Google Scholar
  67. 67.
    Notti A, Fattorini D, Razzetti EM, Regoli F (2007) Bioaccumulation and biotransformation of arsenic in the Mediterranean polychaete Sabella spallanzanii: experimental observations. Environ Toxicol Chem 26:1186–1191CrossRefGoogle Scholar
  68. 68.
    Avila C, Taboada S, Nuñez-Pons L (2008) Antarctic marine chemical ecology: what is next? Mar Ecol 29:1–71CrossRefGoogle Scholar
  69. 69.
    Goerke H, Emrich R, Weber K, Duchene JC (1991) Concentrations and localization of brominated metabolites in the genus Thelepus (Polychaeta, Terebellidae). Comp Biochem Physiol B 99:203–206CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Dipartimento di Scienze della Vita e dell’AmbienteUniversità Politecnica delle MarcheAnconaItaly

Personalised recommendations