Skip to main content

Advertisement

SpringerLink
Log in

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

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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) 49:169–178

    Article  Google Scholar 

  • 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 439–462

    Chapter  Google Scholar 

  • 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 64:2238–2244

    Article  CAS  Google Scholar 

  • Büchel C, Wilhelm C (1993) In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: progress, problems and perspectives. Photochem Photobiol 58:137–148

    Article  Google Scholar 

  • 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 98:34–43

    Article  CAS  PubMed  Google Scholar 

  • Chaloub RM, Reinert F, Nassar CA, Fleury BG, Mantuano DG, Larkum AW (2010) Photosynthetic properties of three Brazilian seaweeds. Braz J Bot 33:371–374

    Article  Google Scholar 

  • Chekroun KB, Baghour M (2013) The role of algae in phytoremediation of heavy metals: a review. J Mater Environ Sci 4:873–880

    Google Scholar 

  • 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 165:91–97

    Article  CAS  PubMed  Google Scholar 

  • 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 1–17

    Google Scholar 

  • David AH, Wen XW, Mark AS, Nicholas SF (1999) Dual-labeling techniques for trace metal biogeochemical investigations in aquatic plankton communities. Aquat Microb Ecol 19:129–138

    Article  Google Scholar 

  • Davis TA, Volesky B, Mucci A (2003) A review of the biochemistry of heavy metal biosorption by brown algae. Water Res 37:4311–4330

    Article  CAS  PubMed  Google Scholar 

  • 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 91:235–239

    Article  CAS  PubMed  Google Scholar 

  • 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 157:78–85

    Article  CAS  Google Scholar 

  • 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 4:14–20

    Article  CAS  Google Scholar 

  • 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 187–208

    Chapter  Google Scholar 

  • Farias S, Smichowski P, Velez D, Montoro R, Curtosi A, Vodopivez C (2007) Total and inorganic arsenic in Antarctic macroalgae. Chemosphere 69:1017–1024

    Article  CAS  PubMed  Google Scholar 

  • 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 29:2489–2502

    Article  CAS  Google Scholar 

  • Ghimire KN, Inoue K, Ohto K, Hayashida T (2008) Adsorption study of metal ions onto crosslinked seaweed Laminaria japonica. Bioresour Technol 99:32–37

    Article  CAS  PubMed  Google Scholar 

  • 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 1777:488–495

    Article  CAS  PubMed  Google Scholar 

  • 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 66:3247–3252

    Article  CAS  Google Scholar 

  • 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 29:903–915

    Article  CAS  Google Scholar 

  • Hashim MA, Chu KH (2004) Biosorption of cadmium by brown, green, and red seaweeds. Chem Eng J 97:249–255

    Article  CAS  Google Scholar 

  • 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 27:169–176

    Article  CAS  PubMed  Google Scholar 

  • Jiang FY, Chen X, Luo AC (2009) Iron plaque formation on wetland plants and its influence on phosphorus, calcium and metal uptake. Aquat Ecol 43:879–890

    Article  CAS  Google Scholar 

  • 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 169:464–470

    Article  CAS  PubMed  Google Scholar 

  • 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 1–96

  • Kittle RP, McDermid KJ (2016) Glyphosate herbicide toxicity to native Hawaiian macroalgal and seagrass species. J Appl Phycol 28:2597–2604

    Article  CAS  Google Scholar 

  • 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 24:2630–2639

    Article  CAS  PubMed  Google Scholar 

  • Li N, Wang J, Song W-Y (2016) Arsenic uptake and translocation in plants. Plant Cell Physiol 57:4–13

    Article  CAS  PubMed  Google Scholar 

  • 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 24:427–432

    Article  Google Scholar 

  • 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 101:5104–5111

    Article  CAS  PubMed  Google Scholar 

  • 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 105:9931–9935

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 497:49–55

    Article  CAS  Google Scholar 

  • 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 8:9–18

    Article  CAS  Google Scholar 

  • Malea P, Kevrekidis T (2014) Trace element patterns in marine macroalgae. Sci Total Environ 494–495:144–157

    Article  CAS  PubMed  Google Scholar 

  • 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 10

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

  • Meharg AA (2004) Arsenic in rice—understanding a new disaster for South-East Asia. Trends Plant Sci 9:415–417

    Article  CAS  PubMed  Google Scholar 

  • Meharg AA, Jardine L (2003) Arsenite transport into paddy rice (Oryza sativa) roots. New Phytol 157:39–44

    Article  CAS  Google Scholar 

  • Meng X, Korfiatis GP, Bang S, Bang KW (2002) Combined effects of anions on arsenic removal by iron hydroxides. Toxicol Lett 133:103–111

    Article  CAS  PubMed  Google Scholar 

  • 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 65:585–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miteva E, Merakchiyska M (2002) Response of chloroplasts and photosynthetic mechanism of bean plants to excess arsenic in soil. Bulg J Agric Sci 8:151–156

    Google Scholar 

  • 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 145–169

  • Mohan D, Pittman CU Jr (2007) Arsenic removal from water/wastewater using adsorbents—a critical review. J Hazard Mater 142:1–53

    Article  CAS  PubMed  Google Scholar 

  • Pennesi C, Vegliò F, Totti C, Romagnoli T, Beolchini F (2012) Nonliving biomass of marine macrophytes as arsenic(V) biosorbents. J Appl Phycol 24:1495–1502

    Article  CAS  Google Scholar 

  • Pinto E, Sigaud-kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal–induced oxidative stress in algae. J Phycol 39:1008–1018

    Article  CAS  Google Scholar 

  • Rahman MA, Hassler C (2014) Is arsenic biotransformation a detoxification mechanism for microorganisms? Aquat Toxicol 146:212–219

    Article  CAS  PubMed  Google Scholar 

  • 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 69:493–499

    Article  CAS  PubMed  Google Scholar 

  • 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 160:356–361

    Article  CAS  PubMed  Google Scholar 

  • 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 145:179–184

    Article  CAS  Google Scholar 

  • Rahman MA, Hasegawa H, Lim RP (2012) Bioaccumulation, biotransformation and trophic transfer of arsenic in the aquatic food chain. Environ Res 116:118–135

    Article  CAS  PubMed  Google Scholar 

  • Raven KP, Jain A, Loeppert RH (1998) Arsenite and arsenate adsorption on ferrihydrite: kinetics, equilibrium, and adsorption envelopes. Environ Sci Technol 32:344–349

    Article  CAS  Google Scholar 

  • 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 58:206–215

    Article  CAS  Google Scholar 

  • 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 45:1263–1267

    Article  CAS  PubMed  Google Scholar 

  • 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 50:117–138

    Article  CAS  Google Scholar 

  • 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 276–351

    Chapter  Google Scholar 

  • 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 49–70

    Chapter  Google Scholar 

  • 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 37:67

    Article  CAS  Google Scholar 

  • Smedley P, Kinniburgh D (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568

    Article  CAS  Google Scholar 

  • 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 25:9708–9721

    Article  CAS  PubMed  Google Scholar 

  • Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409:2430–2442

    Article  CAS  PubMed  Google Scholar 

  • Stoeva N, Berova M, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plant 49:293–296

    Article  CAS  Google Scholar 

  • 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 376:1–19

    Article  Google Scholar 

  • Taylor VF, Jackson BP (2016) Concentrations and speciation of arsenic in New England seaweed species harvested for food and agriculture. Chemosphere 163:6–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:1893–1904

    Article  CAS  Google Scholar 

  • Thursby GB, Steele RL (1984) Toxicity of arsenite and arsenate to the marine macroalga Champia Parvula (Rhodophyta). Environ Toxicol Chem 3:391–397

  • 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 457:173–185

    Article  CAS  Google Scholar 

  • 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 14:427–451

    Article  CAS  Google Scholar 

  • 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 24:21213–21221

    Article  CAS  Google Scholar 

  • Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Graduate School of Natural Science and Technology, Kanazawa University, Kakuma, Kanazawa, 920-1192, Japan

    M. Abdullah Al Mamun, Yoshiki Omori & Rimana Islam Papry

  2. Department of Soil Science, Hajee Mohammad Danesh Science and Technology University, Dinajpur, 5200, Bangladesh

    M. Abdullah Al Mamun

  3. Advanced Technology Research Laboratories, Nippon Steel and Sumitomo Metal Corporation, 20-1 Shintomi, Futtsu City, Chiba, 293-8511, Japan

    Chika Kosugi

  4. Institute of Science and Engineering, Kanazawa University, Kakuma, Kanazawa, 920-1192, Japan

    Osamu Miki, Asami S. Mashio, Teruya Maki & Hiroshi Hasegawa

  5. Institute of Environmental Radioactivity, Fukushima University, 1 Kanayagawa, Fukushima City, Fukushima, 960-1296, Japan

    Ismail M. M. Rahman

Authors
  1. M. Abdullah Al Mamun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoshiki Omori
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rimana Islam Papry
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chika Kosugi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Osamu Miki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ismail M. M. Rahman
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Asami S. Mashio
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Teruya Maki
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hiroshi Hasegawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to M. Abdullah Al Mamun, Ismail M. M. Rahman or Hiroshi Hasegawa.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 1.81 mb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mamun, M.A.A., Omori, Y., Papry, R.I. et al. Bioaccumulation and biotransformation of arsenic by the brown macroalga Sargassum patens C. Agardh in seawater: effects of phosphate and iron ions. J Appl Phycol 31, 2669–2685 (2019). https://doi.org/10.1007/s10811-018-1721-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1721-x

Keywords

Search

Navigation