Advertisement

Bioaccumulation and biotransformation of arsenic by the brown macroalga Sargassum patens C. Agardh in seawater: effects of phosphate and iron ions

  • M. Abdullah Al MamunEmail author
  • Yoshiki Omori
  • Rimana Islam Papry
  • Chika Kosugi
  • Osamu Miki
  • Ismail M. M. RahmanEmail author
  • Asami S. Mashio
  • Teruya Maki
  • Hiroshi HasegawaEmail author
Article

Abstract

The toxicity and bioaccumulation and biotransformation potential of inorganic arsenic (IAs) species As(V) and As(III) were investigated using Sargassum patens under laboratory culture for 7 days. Algal chlorophyll fluorescence decreased with increasing As(V) and As(III) concentrations, being significantly affected by As(III) treatments. Higher As(III) concentration negatively affected growth rate, and P and Fe limitation greatly enhanced IAs toxicity. The extracellular, intracellular, and total bioaccumulation of As(III) and As(V) varied significantly depending on initial concentrations and addition of P and Fe. P and Fe availability suppressed intracellular As accumulation in As(V) medium but not in As(III) medium. In P-rich (10 μmol L−1) medium, intracellular As was reduced by 4.7% and 9.9% when As(V) in the medium was constant (4.0 μmol L−1), under Fe-limited (0 μmol L−1) and Fe-rich (10 μmol L−1) conditions, respectively. However, the Fe-rich condition positively affected extracellular As accumulation from both As source. Extracellular As increased by 43.5% and 38.8% in P-limited + Fe-rich cultures with 4.0 μmol L−1 of As(V) and As(III), respectively. Algae exhibited greater absorption and adsorption to As(V) than to As(III). The reduced metabolites of As(III) (3.5 to 4.9% of the total As) and oxidized metabolites of As(V) (2.0 to 3.7% of the total As) were recorded as biotransformed species from coexisting media containing As(V) and As(III) at a constant 4.0 μmol L−1, respectively. Both P and Fe had significant influences on the variation in behaviors of IAs. This information is vital in terms of As research in marine ecosystems.

Keywords

Bioaccumulation Biotransformation Chlorophyll fluorescence Inorganic As Macroalgae Sargassum patens Phaeophyta 

Notes

Acknowledgements

The study has been partially supported by Grants-in-Aid for Scientific Research (15H05118 and 17K00622) from the Japan Society for the Promotion of Science.

Supplementary material

10811_2018_1721_MOESM1_ESM.docx (1.8 mb)
ESM 1 (DOCX 1.81 mb)

References

  1. Baker J, Wallschlager D (2016) The role of phosphorus in the metabolism of arsenate by a freshwater green alga, Chlorella vulgaris. J Environ Sci (China) 49:169–178CrossRefGoogle Scholar
  2. Bhattacharya P, Chakraborty N, Pal R (2015) Bioremediation of toxic metals using algae. In: Das D (ed) Algal biorefinery: an integrated approach. Springer International Publishing, Cham, pp 439–462CrossRefGoogle Scholar
  3. Brito GB, de Souza TL, Bressy FC, Moura CW, Korn MGA (2012) Levels and spatial distribution of trace elements in macroalgae species from the Todos os Santos Bay, Bahia, Brazil. Mar Poll Bull 64:2238–2244CrossRefGoogle Scholar
  4. Büchel C, Wilhelm C (1993) In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: progress, problems and perspectives. Photochem Photobiol 58:137–148CrossRefGoogle Scholar
  5. Casado-Martinez M, Smith B, Luoma S, Rainbow P (2010) Bioaccumulation of arsenic from water and sediment by a deposit-feeding polychaete (Arenicola marina): a biodynamic modelling approach. Aquat Toxicol 98:34–43CrossRefPubMedGoogle Scholar
  6. Chaloub RM, Reinert F, Nassar CA, Fleury BG, Mantuano DG, Larkum AW (2010) Photosynthetic properties of three Brazilian seaweeds. Braz J Bot 33:371–374CrossRefGoogle Scholar
  7. Chekroun KB, Baghour M (2013) The role of algae in phytoremediation of heavy metals: a review. J Mater Environ Sci 4:873–880Google Scholar
  8. Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97CrossRefPubMedGoogle Scholar
  9. Cosgrove J, Borowitzka MA (2010) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–17Google Scholar
  10. David AH, Wen XW, Mark AS, Nicholas SF (1999) Dual-labeling techniques for trace metal biogeochemical investigations in aquatic plankton communities. Aquat Microb Ecol 19:129–138CrossRefGoogle Scholar
  11. Davis TA, Volesky B, Mucci A (2003) A review of the biochemistry of heavy metal biosorption by brown algae. Water Res 37:4311–4330CrossRefGoogle Scholar
  12. Drličková G, Vaculík M, Matejkovič P, Lux A (2013) Bioavailability and toxicity of arsenic in maize (Zea mays L.) grown in contaminated soils. Bull Environ Contam Toxicol 91:235–239CrossRefGoogle Scholar
  13. Duncan EG, Maher WA, Foster SD, Krikowa F (2013) The influence of arsenate and phosphate exposure on arsenic uptake, metabolism and species formation in the marine phytoplankton Dunaliella tertiolecta. Mar Chem 157:78–85CrossRefGoogle Scholar
  14. Endo H, Suehiro K, Kinoshita J, Gao X, Agatsuma Y (2013) Combined effects of temperature and nutrient availability on growth and phlorotannin concentration of the brown alga Sargassum patens (Fucales; Phaeophyceae). Am J Plant Sci 4:14–20CrossRefGoogle Scholar
  15. Enríquez S, Borowitzka MA (2010) The use of the fluorescence signal in studies of seagrasses and macroalgae. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 187–208CrossRefGoogle Scholar
  16. Farias S, Smichowski P, Velez D, Montoro R, Curtosi A, Vodopivez C (2007) Total and inorganic arsenic in Antarctic macroalgae. Chemosphere 69:1017–1024CrossRefPubMedGoogle Scholar
  17. Farias DR, Hurd CL, Eriksen RS, Simioni C, Schmidt E, Bouzon ZL, Macleod CK (2017) In situ assessment of Ulva australis as a monitoring and management tool for metal pollution. J Appl Phycol 29:2489–2502CrossRefGoogle Scholar
  18. Ghimire KN, Inoue K, Ohto K, Hayashida T (2008) Adsorption study of metal ions onto crosslinked seaweed Laminaria japonica. Bioresour Technol 99:32–37CrossRefPubMedGoogle Scholar
  19. Gong H, Tang Y, Wang J, Wen X, Zhang L, Lu C (2008) Characterization of photosystem II in salt-stressed cyanobacterial Spirulina platensis cells. BBA-Bioenergetics 1777:488–495CrossRefPubMedGoogle Scholar
  20. Hasegawa H, Sohrin Y, Matsui M, Hojo M, Kawashima M (1994) Speciation of arsenic in natural waters by solvent extraction and hydride generation atomic absorption spectrometry. Anal Chem 66:3247–3252CrossRefGoogle Scholar
  21. Hasegawa H, Tate Y, Ogino M, Maki T, Begum ZA, Ichijo T, Rahman IMM (2017) Laboratory culture experiments to study the effect of lignite humic acid fractions on iron solubility and iron uptake rates in phytoplankton. J Appl Phycol 29:903–915CrossRefGoogle Scholar
  22. Hashim MA, Chu KH (2004) Biosorption of cadmium by brown, green, and red seaweeds. Chem Eng J 97:249–255CrossRefGoogle Scholar
  23. Hu Y, Li J-H, Zhu Y-G, Huang Y-Z, Hu H-Q, Christie P (2005) Sequestration of As by iron plaque on the roots of three rice (Oryza sativa L.) cultivars in a low-P soil with or without P fertilizer. Environ Geochem Health 27:169–176CrossRefGoogle Scholar
  24. Jiang FY, Chen X, Luo AC (2009) Iron plaque formation on wetland plants and its influence on phosphorus, calcium and metal uptake. Aquat Ecol 43:879–890CrossRefGoogle Scholar
  25. Khan N, Ryu KY, Choi JY, Nho EY, Habte G, Choi H, Kim MH, Park KS, Kim KS (2015) Determination of toxic heavy metals and speciation of arsenic in seaweeds from South Korea. Food Chem 169:464–470CrossRefGoogle Scholar
  26. Khan N, Seshadri B, Bolan N, Saint CP, Kirkham MB, Chowdhury S, Yamaguchi N, Lee DY, Li G, Kunhikrishnan A, Qi F, Karunanithi R, Qiu R, Zhu YG, Syu CH (2016) Root iron plaque on wetland plants as a dynamic pool of nutrients and contaminants. In: Sparks DL (ed) Advances in agronomy, vol 138. Academic Press, pp 1–96Google Scholar
  27. Kittle RP, McDermid KJ (2016) Glyphosate herbicide toxicity to native Hawaiian macroalgal and seagrass species. J Appl Phycol 28:2597–2604CrossRefGoogle Scholar
  28. Levy JL, Stauber JL, Adams MS, Maher WA, Kirby JK, Jolley DF (2005) Toxicity, biotransformation, and mode of action of arsenic in two freshwater microalgae (Chlorella sp. and Monoraphidium arcuatum). Environ Toxicol Chem 24:2630–2639CrossRefGoogle Scholar
  29. Li N, Wang J, Song W-Y (2016) Arsenic uptake and translocation in plants. Plant Cell Physiol 57:4–13CrossRefGoogle Scholar
  30. Loureiro RR, Reis RP, Berrogain FD, Critchley AT (2012) Extract powder from the brown alga Ascophyllum nodosum (Linnaeus) Le Jolis (AMPEP): a “vaccine-like” effect on Kappaphycus alvarezii (Doty) Doty ex P.C. Silva. J Appl Phycol 24:427–432CrossRefGoogle Scholar
  31. Luna AS, Costa AL, da Costa ACA, Henriques CA (2010) Competitive biosorption of cadmium (II) and zinc (II) ions from binary systems by Sargassum filipendula. Bioresour Technol 101:5104–5111CrossRefGoogle Scholar
  32. Ma JF, Yamaji N, Mitani N, Xu X-Y, Su Y-H, McGrath SP, Zhao F-J (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci U S A 105:9931–9935CrossRefPubMedGoogle Scholar
  33. Ma Z, Lin L, Wu M, Yu H, Shang T, Zhang T, Zhao M (2018) Total and inorganic arsenic contents in seaweeds: absorption, accumulation, transformation and toxicity. Aquaculture 497:49–55CrossRefGoogle Scholar
  34. Maher WA, Foster SD, Taylor AM, Krikowa F, Duncan EG, Chariton AA (2011) Arsenic distribution and species in two Zostera capricorni seagrass ecosystems, New South Wales, Australia. Environ Chem 8:9–18CrossRefGoogle Scholar
  35. Malea P, Kevrekidis T (2014) Trace element patterns in marine macroalgae. Sci Total Environ 494–495:144–157CrossRefGoogle Scholar
  36. Mamun MAA, Datta RR, Kosugi C, Miki O, Oura M, Rahman IMM, Maki T, Hasegawa H (2017) Arsenic speciation and biotransformation by marine macroalgae in seawater. Paper presented at the Asia/CJK Symposium on Analytical Chemistry, Tokyo University of Science, Tokyo, Japan, September 10Google Scholar
  37. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668Google Scholar
  38. Meharg AA (2004) Arsenic in rice—understanding a new disaster for South-East Asia. Trends Plant Sci 9:415–417CrossRefGoogle Scholar
  39. Meharg AA, Jardine L (2003) Arsenite transport into paddy rice (Oryza sativa) roots. New Phytol 157:39–44CrossRefGoogle Scholar
  40. Meng X, Korfiatis GP, Bang S, Bang KW (2002) Combined effects of anions on arsenic removal by iron hydroxides. Toxicol Lett 133:103–111CrossRefPubMedGoogle Scholar
  41. Miller EP, Böttger LH, Weerasinghe AJ, Crumbliss AL, Matzanke BF, Meyer-Klaucke W, Küpper FC, Carrano CJ (2013) Surface-bound iron: a metal ion buffer in the marine brown alga Ectocarpus siliculosus? J Exp Bot 65:585–594CrossRefPubMedGoogle Scholar
  42. Miteva E, Merakchiyska M (2002) Response of chloroplasts and photosynthetic mechanism of bean plants to excess arsenic in soil. Bulg J Agric Sci 8:151–156Google Scholar
  43. Mitra A, Chatterjee S, Gupta DK (2017) Uptake, transport, and remediation of arsenic by algae and higher plants. In: Gupta DK, Chatterjee S (eds) Arsenic contamination in the environment: the issues and solutions. Springer, Cham, pp 145–169Google Scholar
  44. Mohan D, Pittman CU Jr (2007) Arsenic removal from water/wastewater using adsorbents—a critical review. J Hazard Mater 142:1–53CrossRefPubMedGoogle Scholar
  45. Pennesi C, Vegliò F, Totti C, Romagnoli T, Beolchini F (2012) Nonliving biomass of marine macrophytes as arsenic(V) biosorbents. J Appl Phycol 24:1495–1502CrossRefGoogle Scholar
  46. Pinto E, Sigaud-kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal–induced oxidative stress in algae. J Phycol 39:1008–1018CrossRefGoogle Scholar
  47. Rahman MA, Hassler C (2014) Is arsenic biotransformation a detoxification mechanism for microorganisms? Aquat Toxicol 146:212–219CrossRefPubMedGoogle Scholar
  48. Rahman MA, Hasegawa H, Ueda K, Maki T, Okumura C, Rahman MM (2007) Arsenic accumulation in duckweed (Spirodela polyrhiza L.): a good option for phytoremediation. Chemosphere 69:493–499CrossRefPubMedGoogle Scholar
  49. Rahman MA, Hasegawa H, Ueda K, Maki T, Rahman MM (2008a) Arsenic uptake by aquatic macrophyte Spirodela polyrhiza L.: interactions with phosphate and iron. J Hazard Mater 160:356–361CrossRefPubMedGoogle Scholar
  50. Rahman MA, Hasegawa H, Ueda K, Maki T, Rahman MM (2008b) Influence of phosphate and iron ions in selective uptake of arsenic species by water fern (Salvinia natans L.). Chem Eng J 145:179–184CrossRefGoogle Scholar
  51. Rahman MA, Hasegawa H, Lim RP (2012) Bioaccumulation, biotransformation and trophic transfer of arsenic in the aquatic food chain. Environ Res 116:118–135CrossRefGoogle Scholar
  52. Raven KP, Jain A, Loeppert RH (1998) Arsenite and arsenate adsorption on ferrihydrite: kinetics, equilibrium, and adsorption envelopes. Environ Sci Technol 32:344–349CrossRefGoogle Scholar
  53. Robinson B, Kim N, Marchetti M, Moni C, Schroeter L, van den Dijssel C, Milne G, Clothier B (2006) Arsenic hyperaccumulation by aquatic macrophytes in the Taupo volcanic zone, New Zealand. Environ Exp Bot 58:206–215CrossRefGoogle Scholar
  54. Rose M, Lewis J, Langford N, Baxter M, Origgi S, Barber M, MacBain H, Thomas K (2007) Arsenic in seaweed--forms, concentration and dietary exposure. Food Chem Toxicol 45:1263–1267CrossRefGoogle Scholar
  55. Rue EL, Bruland KW (1995) Complexation of iron (III) by natural organic ligands in the central North Pacific as determined by a new competitive ligand equilibration/adsorptive cathodic stripping voltammetric method. Mar Chem 50:117–138CrossRefGoogle Scholar
  56. Sartal CG, Alonso MCB, Barrera PB (2014) Arsenic in seaweed: presence, bioavailability and speciation. In: Kim S-K (ed) Seafood science: advances in chemistry, Technology and Applications. CRC Press, Boca Raton, pp 276–351CrossRefGoogle Scholar
  57. Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 49–70CrossRefGoogle Scholar
  58. Shaibur MR, Huq SI, Kawai S (2015) Quantitative analysis of phosphorus, iron, and arsenic in the inner and outer portions of rice roots: an interaction of arsenic with iron. Acta Physiol Plant 37:67CrossRefGoogle Scholar
  59. Smedley P, Kinniburgh D (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568CrossRefGoogle Scholar
  60. Squadrone S, Brizio P, Battuello M, Nurra N, Sartor RM, Riva A, Staiti M, Benedetto A, Pessani D, Abete MC (2018) Trace metal occurrence in Mediterranean seaweeds. Environ Sci Pollut Res Int 25:9708–9721CrossRefGoogle Scholar
  61. Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409:2430–2442CrossRefGoogle Scholar
  62. Stoeva N, Berova M, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plant 49:293–296CrossRefGoogle Scholar
  63. Suggett DJ, Moore CM, Hickman AE, Geider RJ (2009) Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state. Mar Ecol Prog Ser 376:1–19CrossRefGoogle Scholar
  64. Taylor VF, Jackson BP (2016) Concentrations and speciation of arsenic in New England seaweed species harvested for food and agriculture. Chemosphere 163:6–13CrossRefPubMedGoogle Scholar
  65. Terada R, Matsumoto K, Borlongan IA, Watanabe Y, Nishihara GN, Endo H, Shimada S (2018) The combined effects of PAR and temperature including the chilling-light stress on the photosynthesis of a temperate brown alga, Sargassum patens (Fucales), based on field and laboratory measurements. J Appl Phycol 30:1893–1904CrossRefGoogle Scholar
  66. Thursby GB, Steele RL (1984) Toxicity of arsenite and arsenate to the marine macroalga Champia Parvula (Rhodophyta). Environ Toxicol Chem 3:391–397Google Scholar
  67. Tukai R, Maher WA, McNaught IJ, Ellwood MJ (2002) Measurement of arsenic species in marine macroalgae by microwave-assisted extraction and high performance liquid chromatography–inductively coupled plasma mass spectrometry. Anal Chim Acta 457:173–185CrossRefGoogle Scholar
  68. Wang Y, Wang S, Xu P, Liu C, Liu M, Wang Y, Wang C, Zhang C, Ge Y (2015) Review of arsenic speciation, toxicity and metabolism in microalgae. Rev Environ Sci Biotechnol 14:427–451CrossRefGoogle Scholar
  69. Wang Y, Zhang C, Zheng Y, Ge Y (2017) Bioaccumulation kinetics of arsenite and arsenate in Dunaliella salina under different phosphate regimes. Environ Sci Pollut Res 24:21213–21221CrossRefGoogle Scholar
  70. Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Graduate School of Natural Science and TechnologyKanazawa UniversityKanazawaJapan
  2. 2.Department of Soil ScienceHajee Mohammad Danesh Science and Technology UniversityDinajpurBangladesh
  3. 3.Advanced Technology Research Laboratories, Nippon Steel and Sumitomo Metal CorporationFuttsu CityJapan
  4. 4.Institute of Science and EngineeringKanazawa UniversityKanazawaJapan
  5. 5.Institute of Environmental RadioactivityFukushima UniversityFukushima CityJapan

Personalised recommendations