Arsenic is not stored as arsenite–phytochelatin complexes in the seaweeds Fucus spiralis and Hizikia fusiforme

B. Alan Wood; Shinichi Miyashita; Toshikazu Kaise; Andrea Raab; Andrew A. Meharg; Jörg Feldmann

doi:10.1071/EN10071

RESEARCH ARTICLE

Arsenic is not stored as arsenite–phytochelatin complexes in the seaweeds Fucus spiralis and Hizikia fusiforme

B. Alan Wood ^A , Shinichi Miyashita ^B , Toshikazu Kaise ^B , Andrea Raab ^A , Andrew A. Meharg ^C and Jörg Feldmann ^A ^D

+ Author Affiliations

- Author Affiliations

^A Trace Element Speciation Laboratory (TESLA), Department of Chemistry, University of Aberdeen, Meston Walk, Aberdeen, AB24 3UE, Scotland, UK.

^B School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Horinouchi 1432-1, Hachioji, Tokyo 192-0392, Japan.

^C School of Biological Sciences, University of Aberdeen, Aberdeen, AB24 3UU, Scotland, UK.

^D Corresponding author. Email: j.feldmann@abdn.ac.uk

We dedicate this paper to the memory of the late Professor Kaise in recognition of his lifelong work on environmental arsenic chemistry.

Environmental Chemistry 8(1) 30-43 https://doi.org/10.1071/EN10071
Submitted: 3 July 2010 Accepted: 21 September 2010 Published: 28 February 2011

Environmental context. Seaweeds hyperaccumulate the toxic metalloid arsenic, but seemingly achieve detoxification by transformation to arsenosugars. The edible seaweed hijiki is a notable exception because it contains high levels of toxic arsenate and arsenite. Terrestrial plants detoxify arsenic by forming arsenite–phytochelatin complexes. The hypothesis that seaweeds also synthesise phytochelatins to bind arsenite as a means of detoxification before arsenosugar synthesis is tested in this investigation.

Abstract. Phytochelatins (PCs), generic structure [γ-Glu-Cys]n-Gly, are peptides synthesised by terrestrial plants to bind toxic metal(loid)s such as cadmium and arsenic. Seaweeds are arsenic hyperaccumulators, seemingly achieving detoxification via arsenosugar biosynthesis. Whether seaweeds synthesise PCs to aid detoxification during arsenic exposure is unknown. Hizikia fusiforme (hijiki) and Fucus spiralis were used as model seaweeds: the former is known for its large inorganic arsenic concentration, whereas the latter contains mainly arsenosugars. F. spiralis was exposed to 0, 1 and 10 mg L^–1 arsenate solutions for 24 h, whereas hijiki was analysed fresh. All samples contained As^III, glutathione and reduced PC₂, identified using HPLC-ICP-MS/ES-MS. Although hijiki contained no As^III–PC complexes, arsenate exposed F. spiralis generated traces of numerous arsenic compounds that might be As^III–GS or As^III–PC₂ complexes. As^III–PC complexes seem not to be a principal storage form for long-term arsenic storage within seaweeds. However, 40 times higher glutathione concentrations were found in hijiki than F. spiralis, which may explain how hijiki deals with its high inorganic arsenic burden.

Additional keywords: arsenosugars, detoxification, hijiki.

References

[1] W. Zeng, B. Hemmasi, Solution synthesis of phytochelatins, isopeptides from the plant kingdom. Liebigs Ann. Chem. 1992, 311.
| Solution synthesis of phytochelatins, isopeptides from the plant kingdom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XitFCrtbc%3D&md5=0b5cdfed01ccc558640848c2a3bb1f95CAS |

[2] R. Kneer, T. M. Kutchan, A. Hochberger, M. H. Zenk, Saccharomyces cerevisiae and Neurospora crassa contain heavy metal sequestering phytochelatin. Arch. Microbiol. 1992, 157, 305.
| Saccharomyces cerevisiae and Neurospora crassa contain heavy metal sequestering phytochelatin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XisFSitb4%3D&md5=fdc748a04a74100dd588fe0fdc835d85CAS | 1534214PubMed |

[3] M. H. Zenk, Heavy metal detoxification in higher plants – a review. Gene 1996, 179, 21.
| Heavy metal detoxification in higher plants – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xnt1WisL0%3D&md5=af540999d4b2174cf9ee5f1530d3bcdbCAS | 8955625PubMed |

[4] W. E. Rauser, Phytochelatins and related peptides – structure, biosynthesis and function. Plant Physiol. 1995, 109, 1141.
| Phytochelatins and related peptides – structure, biosynthesis and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSnsb7M&md5=29ce2ee243bf6800ec0b8ea880443b88CAS | 8539285PubMed |

[6] M. E. V. Schmöger, M. Oven, E. Grill, Detoxification of arsenic by phytochelatins in plants. Plant Physiol. 2000, 122, 793.
| Detoxification of arsenic by phytochelatins in plants.Crossref | GoogleScholarGoogle Scholar | 10712543PubMed |

[7] A. A. Meharg, M. R. MacNair, An altered phosphate uptake system in arsenate-tolerant Holcus Lanatus L. New Phytol. 1990, 116, 29.
| An altered phosphate uptake system in arsenate-tolerant Holcus Lanatus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXnvVOhsA%3D%3D&md5=d2c4a6fd55f7a9fd5c5f0a0945214140CAS |

[8] A. A. Meharg, M. R. MacNair, Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus Lanatus L. J. Exp. Bot. 1992, 43, 519.
| Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus Lanatus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XisFSis7Y%3D&md5=2116b7ab2b7520b3bd71c5dbd396e131CAS |

[9] C. S. Cobbett, Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 2000, 123, 825.
| Phytochelatins and their roles in heavy metal detoxification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1SlsLY%3D&md5=07885b9213fe434cd16aaeb22a41aefdCAS | 10889232PubMed |

[10] E. Lombi, F. J. Zhao, M. Fuhrmann, L. Q. Ma, S. P. McGrath, Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol. 2002, 156, 195.
| Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFGru7g%3D&md5=5f5284159e5dfc4fd67f8ed09c15f345CAS |

[11] J. Wang, F. J. Zhao, A. A. Meharg, A. Raab, J. Feldmann, S. P. McGrath, Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol. 2002, 130, 1552.
| Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVOmsbY%3D&md5=2a409384c0ad54b13e2a0641d6ac8670CAS | 12428020PubMed |

[12] C. Tu, L. Q. Ma, B. Bondada, Arsenic accumulation in the hyperaccumulator chinese brake and its utilisation potential for phytoremediation. J. Environ. Qual. 2002, 31, 1671.
| Arsenic accumulation in the hyperaccumulator chinese brake and its utilisation potential for phytoremediation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsFemsbs%3D&md5=f6016d3995e39fbbf77eb17ae1ebe148CAS | 12371185PubMed |

[13] J. Johanning, H. Strasdeit, A coordination-chemical basis for the biological function of the phytochelatins. Angew. Chem. Int. Ed. 1998, 37, 2464.
| A coordination-chemical basis for the biological function of the phytochelatins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntVSiu7g%3D&md5=1f7a719e3b26cf11d09c82b4d64ef221CAS |

[14] R. Kneer, M. H. Zenk, The formation of Cd–phytochelatin complexes in plant cell cultures. Phytochemistry 1997, 44, 69.
| The formation of Cd–phytochelatin complexes in plant cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsVSrsw%3D%3D&md5=f3cffb234223f663879352815ebca061CAS |

[15] W. J. Liu, B. A. Wood, A. Raab, S. P. McGrath, F. J. Zhao, J. Feldmann, Complexation of arsenite with phytochelatins reduces arsenic efflux and translocation from roots to shoots in Arabidopsis. New Phytol. 2010, 152, 2211..

[16] J. L. Gómez-Ariza, D. Sanchez-Rodas, I. Giraldez, E. Morales, A comparison between ICP-MS and AFS detection for arsenic speciation in environmental samples. Talanta 2000, 51, 257.
| A comparison between ICP-MS and AFS detection for arsenic speciation in environmental samples.Crossref | GoogleScholarGoogle Scholar | 18967857PubMed |

[17] W. R. G. Atkins, E. G. Wilson, The phosphorus and arsenic compounds of seawater. J. Mar. Biol. Assoc. U. K. 1927, 14, 609.
| The phosphorus and arsenic compounds of seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaB2sXhtlKrsQ%3D%3D&md5=ed24feeecc72e02413090995e089f584CAS |

[18] C. Almela, J. M. Laparra, D. Viez, R. Barber, R. Farr, R. Montoro, Arsenosugars in raw and cooked edible seaweed: characterisation and bioaccessibility. J. Agric. Food Chem. 2005, 53, 7344.
| Arsenosugars in raw and cooked edible seaweed: characterisation and bioaccessibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXns1ait7o%3D&md5=790207c2f076926dd22b225eb626e522CAS | 16131152PubMed |

[19] J. Feldmann, K. John, P. Pengprecha, Arsenic metabolism in seaweed-eating sheep from Northern Scotland. Fresenius J. Anal. Chem. 2000, 368, 116.
| Arsenic metabolism in seaweed-eating sheep from Northern Scotland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlslKrurg%3D&md5=e454eaf9a305d35ac9398768e1a3d12fCAS | 11220824PubMed |

[20] S. McSheehy, M. Marcinek, H. Chassaigne, J. Szpunar, Identification of dimethylarsinoyl-riboside derivatives in seaweed by pneumatically assisted electrospray tandem mass spectrometry. Anal. Chim. Acta 2000, 410, 71.
| Identification of dimethylarsinoyl-riboside derivatives in seaweed by pneumatically assisted electrospray tandem mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitVSmu7k%3D&md5=f50d9c5b3cee746c2f8a5fcccb0bff78CAS |

[21] P. Andrewes, D. M. Demarini, K. Funaska, K. Wallace, V. W. M. Lai, H. Sun, W. R. Cullen, K. T. Kitchin, Do arsenosugars pose a risk to human health? The comparative toxicities of a trivalent and pentavalent arsenosugar. Environ. Sci. Technol. 2004, 38, 4140.
| Do arsenosugars pose a risk to human health? The comparative toxicities of a trivalent and pentavalent arsenosugar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsF2itLw%3D&md5=4ad826388efb6060f4e68d25bcffe63eCAS | 15352453PubMed |

[22] F. Challenger, Biological methylation. Chem. Rev. 1945, 36, 315.
| Biological methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH2MXisFGrtQ%3D%3D&md5=86537b05dfe94a77d9ebc74199bd310eCAS |

[23] J. S. Edmonds, K. A. Francesconi, Transformations of arsenic in the marine environment. Experientia 1987, 43, 553.
| Transformations of arsenic in the marine environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXltFaqtrc%3D&md5=acaf0975031bb7d31a8951e11828ada3CAS | 3556209PubMed |

[24] I. Koch, K. McPherson, P. Smith, L. Easton, K. G. Doe, K. J. Reimer, Arsenic bioaccessibility and speciation in clams and seaweed from a contaminated marine environment. Mar. Pollut. Bull. 2007, 54, 586.
| Arsenic bioaccessibility and speciation in clams and seaweed from a contaminated marine environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Sgt70%3D&md5=72d55d4a65e7b6b1cda7da0965426fceCAS | 17241645PubMed |

[25] A. Raab, P. Fecher, J. Feldmann, Determination of arsenic in algae – results of an interlaboratory trial: determination of arsenic species in the water-soluble fraction. Mikrochim. Acta 2005, 151, 153.
| Determination of arsenic in algae – results of an interlaboratory trial: determination of arsenic species in the water-soluble fraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFKht7%2FO&md5=0209829e8ce3139ec22852822256788dCAS |

[26] B. Pawlik-Skowrońska, J. Pirszel, M. T. Brown, Concentrations of phytochelatins and glutathione found in natural assemblages of seaweeds depend on species and metal concentrations of the habitat. Aquat. Toxicol. 2007, 83, 190.
| Concentrations of phytochelatins and glutathione found in natural assemblages of seaweeds depend on species and metal concentrations of the habitat.Crossref | GoogleScholarGoogle Scholar | 17532484PubMed |

[27] A. Raab, P. N. Williams, A. A. Meharg, J. Feldmann, Uptake and translocation of inorganic and methylated arsenic species by plants. Environ. Chem. 2007, 4, 197.
| Uptake and translocation of inorganic and methylated arsenic species by plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvFaltro%3D&md5=24cf25f4a55ddf982a56faf09935b8aaCAS |

[28] K. Bluemlein, A. Raab, A. A. Meharg, J. M. Charnock, J. Feldmann, Can we trust mass spectrometry for determination of arsenic peptides in plants: comparison of LC–ICP-MS and LC-ES-MS/ICP-MS with XANES/EXAFS in analysis of Thunbergia alata. Anal. Bioanal. Chem. 2008, 390, 1739.
| Can we trust mass spectrometry for determination of arsenic peptides in plants: comparison of LC–ICP-MS and LC-ES-MS/ICP-MS with XANES/EXAFS in analysis of Thunbergia alata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsFWrsrw%3D&md5=58415ad8ece28b51511840e0a35eba18CAS | 18084749PubMed |

[29] K. Bluemlein, E. M. Krupp, J. Feldmann, Advantages and limitations of a desolvation system coupled online to HPLC-ICPqMS/ES-MS for the quantitative determination of sulfur and arsenic in arseno-peptide complexes. J. Anal. At. Spectrom. 2009, 24, 108.
| Advantages and limitations of a desolvation system coupled online to HPLC-ICPqMS/ES-MS for the quantitative determination of sulfur and arsenic in arseno-peptide complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWisr%2FE&md5=e4e731c6a37c78eea27ad799e697ab58CAS |

[30] H. Castlehouse, C. Smith, A. Raab, C. Deacon, A. A. Meharg, J. Feldmann, Biotransformation and accumulation of arsenic in soil amended with seaweed. Environ. Sci. Technol. 2003, 37, 951.
| Biotransformation and accumulation of arsenic in soil amended with seaweed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnslyltA%3D%3D&md5=f125d2f2dbc8d42a8fa65108bd42c4d4CAS | 12666926PubMed |

[31] A. Geiszinger, W. Goessler, S. N. Pedersen, K. A. Francesconi, Arsenic biotransformation by the brown macroalga Fucus serratus. Environ. Toxicol. Chem. 2001, 20, 2255..
| 11596758PubMed |

[32] S. C. R. Granchinho, E. Polishchuk, W. R. Cullen, K. J. Reimer, Biomethylation and bioaccumulation of arsenic(V) by marine alga Fucus gardneri. Appl. Organomet. Chem. 2001, 15, 553.
| Biomethylation and bioaccumulation of arsenic(V) by marine alga Fucus gardneri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktFOqsLs%3D&md5=f8cd8a47adb440f686af73c024125707CAS |

[33] S. C. R. Granchinho, C. M. Franz, E. Polishchuk, W. R. Cullen, K. J. Reimer, Transformation of arsenic(V) by the fungus Fusarium oxysporum melonis isolated from the alga Fucus gardneri. Appl. Organomet. Chem. 2002, 16, 721.
| Transformation of arsenic(V) by the fungus Fusarium oxysporum melonis isolated from the alga Fucus gardneri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpslWmtrk%3D&md5=8d61a08a0e2e16c74109efc04e70dd23CAS |

[34] L. A. Murray, A. Raab, I. L. Marr, J. Feldmann, Biotransformation of arsenate to arsenosugars by Chlorella vulgaris. Appl. Organomet. Chem. 2003, 17, 669.
| Biotransformation of arsenate to arsenosugars by Chlorella vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFOrtL4%3D&md5=bc3dcac43ecf61409bccdd26aae7ff90CAS |

[35] A. Raab, A. A. Meharg, M. Jaspars, D. R. Genney, J. Feldmann, Arsenic-glutathione complexes – their stability in solution and during separation by different HPLC modes. J. Anal. At. Spectrom. 2004, 19, 183.
| Arsenic-glutathione complexes – their stability in solution and during separation by different HPLC modes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjslejsA%3D%3D&md5=f66709bca7c14b668f18818bc0db1311CAS |

[36] M. E. Merrifield, T. Ngu, M. J. Stillman, Arsenic binding to Fucus vesiculosus metallothionein. Biochem. Biophys. Res. Commun. 2004, 324, 127.
| Arsenic binding to Fucus vesiculosus metallothionein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1WksLc%3D&md5=65ebbedf2517a01d785cd5c81d8bafe4CAS | 15464992PubMed |

[37] A. Raab, K. Ferreira, A. A. Meharg, J. Feldmann, Can arsenic–phytochelatin complex formation be used as an indicator for toxicity in Helianthus annuus? J. Exp. Bot. 2007, 58, 1333.
| Can arsenic–phytochelatin complex formation be used as an indicator for toxicity in Helianthus annuus?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvFGisrc%3D&md5=02731f8caa15eb0963d3f074dd42ffb5CAS | 17283372PubMed |

[38] F. J. Zhao, J. R. Wang, J. H. A. Barker, H. Schat, P. M. Bleeker, S. P. McGrath, The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol. 2003, 159, 403.
| The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsl2rsL0%3D&md5=e248563e00b51ec5ec30a847ca0f5de9CAS |

[39] A. Raab, J. Feldmann, A. A. Meharg, The nature of arsenic–phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol. 2004, 134, 1113.
| The nature of arsenic–phytochelatin complexes in Holcus lanatus and Pteris cretica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1SjtL8%3D&md5=7675ccb080c8dd04cec91e164061eda5CAS | 15001701PubMed |

Arsenic is not stored as arsenite–phytochelatin complexes in the seaweeds Fucus spiralis and Hizikia fusiforme

References

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