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Accumulation of silver by Fucus spp. (Phaeophyceae) and its toxicity to Fucus ceranoides under different salinity regimes

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Abstract

Metals constitute an important group of abiotic stressors that elicit stress responses in marine algae that include the production of reactive oxygen species (ROS). Silver (Ag) is a highly toxic metal to organisms but despite this there are relatively few studies on how it affects marine macroalgae (seaweeds). In a landmark study published in 1977 the first information was provided on the accumulation of Ag in Fucus spp. (Phaeophyceae) from the Looe estuary, located in south-west England, an area with a long history of mining activity. In the present study, the estuary has been re-visited and the patterns of Ag accumulation in two Fucus spp. and sediment re-examined after 35 years. We conclude that Ag concentrations in sediment and macroalgae from specific sites within the catchment remain high, but more generally sediment concentrations have declined by approximately 65 % and the dissolved, bioavailable fraction by 24 % over this period. In addition, from laboratory studies we provide data on the speciation and toxic effects of Ag under different salinity regimes in the euryhaline brown seaweed, Fucus ceranoides. From these exposure experiments, it was found that with increasing Ag concentrations growth was inhibited and lipid peroxidation associated with ROS production increased. The magnitude of the toxic effects was greater at a salinity of 10 than 28 psu which reflects the greater bioavailability of the toxic species of Ag (Ag+ and AgCl0) at reduced salinities. These findings emphasise the importance of investigating the effects of metal pollution in conjunction with other, natural, environmental stressors such as salinity.

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References

  • Barreiro R, Picaldo L, Real C (2002) Biomonitoring heavy metals in estuaries: a field comparison of two brown algae species inhabiting upper estuarine reaches. Environ Monit Assess 75:121–134. doi:10.1023/A:1014479612811

    Article  CAS  Google Scholar 

  • Brown MT, Newman JE (2003) Physiological responses of Gracilariopsis longissima (S.G. Gmelin) Steentoft, L.M. Irvine and Farnham (Rhodophyceae) to sub-lethal copper concentrations. Aquat Toxicol 64:201–213. doi:10.1016/S0166-445X(03)00054-7

    Article  CAS  Google Scholar 

  • Bryan GW (1983) Brown seaweed, Fucus vesiculosus, and the gastropod, Littorina littorea, as indicators of trace-metal availability in estuaries. Sci Total Environ 28:91–104. doi:10.1016/S0048-9697(83)80010-2

    Article  CAS  Google Scholar 

  • Bryan GW (1984) Pollution due to heavy metals and their compounds. In: Kinne O (ed) Marine ecology part 3. Wiley, London, pp 1289–1430

    Google Scholar 

  • Bryan GW, Gibbs PE (1983) Heavy metals in the Fal Estuary, Cornwall: a study of long-term contamination by mining waste and its effects on estuarine organisms. Occas Publ Mar Biol Assoc UK 2:1–112

    Google Scholar 

  • Bryan GW, Hummerstone LG (1977) Indicators of heavy metal contamination in the Looe Estuary (Cornwall) with particular regard to silver and lead. J Mar Biol Assoc UK 57:75–92. doi:10.1017/S002531540002124X

  • Burzynski M, Zurek A (2007) Effects of copper and cadmium on photosynthesis in cucumber cotyledons. Photosynthetica 45:239–244. doi:10.1007/s11099-007-0038-9

    Article  CAS  Google Scholar 

  • Cain DJ, Luoma SN, Wallace WG (2004) Linking metal bioaccumulation of aquatic insects to their distribution patterns in a mining-impacted river. Environ Toxicol Chem 23:1463–1473. doi:10.1897/03-291

    Article  CAS  Google Scholar 

  • Cairrao E, Couderchet M, Soares AMVM, Guilhermino L (2004) Glutathione-S-transferase activity of Fucus spp. as a biomarker of environmental contamination. Aquat Toxicol 70:277–286. doi:10.1016/j.aquatox.2004.09.005

    Article  CAS  Google Scholar 

  • Collen J, Davison IR (1999) Reactive oxygen production and damage in intertidal Fucus Spp. (Phaeophyceae). J Phycol 35:54–61. doi:10.1046/j.1529-8817.1999.3510054.x

    Article  CAS  Google Scholar 

  • Dewey H (1921) Lead, silver-lead and zinc ores of Cornwall, Devon and Somerset. Economic Memoirs (Special Reports on Mineral Resources), Geological Survey of the United Kingdom 21, 72

  • Esposito A, Pagnanelli F, Lodi A, Soliso C, Veglio F (2001) Biosorption of heavy metals by Sphaerotilus natans: an equilibrium study at different pH and biomass concentrations. Hydrometallurgy 60:129–141. doi:10.1016/S0304-386X(00)00195-X

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Clarendon Press, Oxford

  • Han T, Kang SH, Park JS, Lee HK, Brown MT (2008) Physiological responses of Ulva pertusa and U. armoricana to copper exposure. Aquat Toxicol 86:176–184. doi:10.1016/j.aquatox.2007.10.016

    Article  CAS  Google Scholar 

  • Hellebust JA (1976) Osmoregulation. Annu Rev Plant Physiol 27:485–505

    Article  CAS  Google Scholar 

  • Huang J, Redmann RE (1995) Responses of growth, morphology, and anatomy to salinity and calcium supply in cultivated and wild barley. Can J Bot 73:1859–1866. doi:10.1139/b95-198

    Article  CAS  Google Scholar 

  • Khfaji AK, Norton TA (1979) The effects of salinity on the distribution of Fucus ceranoides. Estuar Coast Mar Sci 8:433–439. doi:10.1016/0302-3524(79)90060-4

    Article  Google Scholar 

  • Langston WJ, Chesman BS, Burt GR, Hawkins SJ, Readman J, Worsfold P (2003) Characterisation of the South West European Marine Sites: Plymouth Sound and Estuaries cSAC, SPA. Marine Biological Association, Plymouth

    Google Scholar 

  • Li R, Brawley SH (2004) Improved survival under heat stress in intertidal embryos (Fucus spp.) simultaneously exposed to hypersalinity and the effect of parental thermal history. Mar Biol 144:205–213. doi:10.1007/s00227-003-1190-9

    Article  Google Scholar 

  • Luoma SN (2008) Silver nanotechnologies and the environment: old problems or new challenges? Project on emerging nanotechnologies

  • Luoma SN, Ho YB, Bryan GW (1995) Fate, bioavailability and toxicity of silver in estuarine environments. Mar Pollut Bull 31:44–54. doi:10.1016/0025-326X(95)00081-W

    Article  CAS  Google Scholar 

  • Maharana D, Jena K, Pise NM, Jagtap TG (2010) Assessment of oxidative stress indices in a marine macro brown alga Padina tetrastromatica (Hauck) from comparable polluted coastal regions of the Arabian Sea, West coast of India. J Environ Sci 22:1413–1418. doi:10.1016/S1001-0742(09)60268-0

    Article  CAS  Google Scholar 

  • Mamboya FA (2007) Heavy metal contamination and toxicity, studies of macroalgae from the Tanzanian Coast: 1–48. Stockholm University

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. doi:10.1093/jexbot/51.345.659

    Article  CAS  Google Scholar 

  • Morel FMM, Reuter JG, Anderson DM, Guillard RRL (1979) Aquil- chemically defined phytoplankton culture-medium for trace-metal studies. J Phycol 15:135–141. doi:10.1111/j.1529-8817.1979.tb02976.x

    Article  CAS  Google Scholar 

  • Navabpour S, Morris K, Allen R, Harrison E, Mackerness SAH, Buchanan- Wollaston V (2003) Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot 54:2285–2292. doi:10.1093/jxb/erg267

    Article  CAS  Google Scholar 

  • Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R (2008) Toxicity of Silver Nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–8964. doi:10.1021/es801785m

    Article  CAS  Google Scholar 

  • Pinto E, Sigaud-Kutner TCS, Leitao MAS, Okamotmo OK, Morse D, Colepicolo P (2003) Heavy metal induces oxidative stress in algae. J Phycol 39:1008–1018. doi:10.1111/j.0022-3646.2003.02-193.x

    Article  CAS  Google Scholar 

  • Price NM, Harrison GI, Hering JG, Hudson RJ, Nirel PMV, Palenik B, Morel FMM (1989) Preparation and chemistry of the artificial algal culture medium Aquil. Biol Oceanogr 6:443–461. doi:10.1080/01965581

    Google Scholar 

  • Rai LC, Gaur JP, Kumar HD (2008) Phycology and heavy metal pollution. Biol Rev 56:99–151. doi:10.1111/j.1469-185X.1981.tb00345.x

    Article  Google Scholar 

  • Rainbow PS, Kriefman S, Smith BD, Luoma SN (2011) Have the bioavailabilities of trace metals to a suite of biomonitors changed over three decades in SW England estuaries historically affected by mining. Sci Total Environ 409:1589–1602. doi:10.1016/j.scitotenv.2011.01.012

    Article  CAS  Google Scholar 

  • Ralph PJ, Smith RA, Macinnis-Ng CMO, Seery CR (2007) Use of fluorescence-based ecotoxicological bioassays in monitoring toxicants and pollution in aquatic systems: review. Toxicol Environ Chem 89:589–607. doi:10.1080/02772240701561593

    Article  CAS  Google Scholar 

  • Ratte HT (1999) Bioaccumulation and toxicity of silver compounds: a review. Environ Toxicol Chem 18:89–108. doi:10.1002/etc.5620180112

    Article  CAS  Google Scholar 

  • Salgado LT, Andrade LR, Amado-Filho GM (2005) Localization of specific monosaccharide in cells of the brown alga Padina gymnospora and the relation to heavy-metal accumulation. Protoplasma 225:123–128. doi:10.1007/s00709-004-0066-2

    Article  CAS  Google Scholar 

  • Suter GW, Lewis MA (1989) Silver transport and impact in estuarine and marine systems. In: Aquatic toxicology and environmental fate, vol 11, pp 5–18. ASTM STP 1007, Philadelphia

  • Szivak I, Behra R, Sigg L (2009) Metal induced reactive oxygen species production in Chlamydomonas reinhardtii (Chlorophyceae). J Phycol 45:427–435. doi:10.1111/j.1529-8817.2009.00663.x

    Article  CAS  Google Scholar 

  • Tappin AD, Barriada JL, Braungardt CB, Evans EH, Patey MD, Achterberg EP (2010) Dissolved silver in European estuarine and coastal waters. Water Res 44:4204–4216. doi:10.1016/j.watres.2010.05.022

    Article  CAS  Google Scholar 

  • Tipping E (1998) Humic ion-binding model VI: an improved description of the interactions of protons and metal ions with humic substances. Aquat Geochem 4:3–47. doi:10.1023/a:1009627214459

    Article  CAS  Google Scholar 

  • Turner A, Brice D, Brown MT (2012) Interactions of silver nanoparticles with the marine macroalga, Ulva lactuca. Ecotoxicology 21:148–154. doi:10.1007/s10646-011-0774-2

    Article  CAS  Google Scholar 

  • Varma R, Turner A, Brown MT (2011) Bioaccumulation of metals by Fucus ceranoides in estuaries of South West England. Mar Pollut Bull 62:2557–2562. doi:10.1016/j.marpolbul.2011.08.016

    Article  CAS  Google Scholar 

  • Varma R, Turner A, Brown MT, Millward GE (2013) Metal accumulation kinetics by the estuarine macroalga, Fucus ceranoides. Estuar Coast Shelf Sci 128:33–40. doi:10.1016/j.ecss.2013.05.014

    Article  CAS  Google Scholar 

  • Vass I, Kirilovsky D, Perewoska I, Máté Z, Nagy F, Etienne AL (2000) UV-B radiation induced exchange of the D1 reaction centre subunits produced from the psbA2 and psbA3 genes in the Cyanobacterium synechocystis sp. PCC 6803. Eur J Biochem 167:2640–2648. doi:10.1046/j.1432-1327.2000.01274.x

    Article  Google Scholar 

  • Wood CM, Grosell M, McDonald MD, Playle RC, Walsh PJ (2010) 532 Effects of waterborne silver in a marine teleost, the gulf toadfish533 (Opsanus beta): effects of feeding and chronic exposure on bioaccumulation. Aquat Toxicol 99:138–148. doi:10.1016/j.aquatox.2010.04.012

    Article  CAS  Google Scholar 

  • Ye J, Li Y, Teruya K, Katakura Y, Ichikawa A, Eto H, Hosoi M, Nishimoto S, Shirahata S (2005) Enzyme-digested fucoidan extracts derived from seaweed Mozuku of Cladosiphon novae-caledoniae kylin inhibit invasion and angiogenesis of tumour cells. Cytotechnology 47:117–126. doi:10.1007/s10616-005-3761-8

    Article  Google Scholar 

  • Zhang ZS, Yang C, Gao HY, Zhang LT, Fan XL, Liu MJ (2014) The higher sensitivity of PSI to ROS results in lower chilling–light tolerance of photosystems in young leaves of cucumber. J Photochem Photobiol B 137:127–134. doi:10.1016/j.jphotobiol.2013.12.012

    Article  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge technical support provided by Angela Harrop, Andrew Atfield and Andrew Fisher.

Conflict of interest

The authors declare that they have no conflicts of interest.

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Authors and Affiliations

  1. GEOMAR Helmholtz Centre for Ocean Research, 2 Hohenbergstraße, 24105, Kiel, Germany

    K. Ramesh

  2. School of Marine Science and Engineering, Plymouth University, Drake Circus, Plymouth, Devon, PL4 8AA, UK

    S. Berry & M. T. Brown

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  1. K. Ramesh
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Correspondence to K. Ramesh.

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Ramesh, K., Berry, S. & Brown, M.T. Accumulation of silver by Fucus spp. (Phaeophyceae) and its toxicity to Fucus ceranoides under different salinity regimes. Ecotoxicology 24, 1250–1258 (2015). https://doi.org/10.1007/s10646-015-1495-8

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