Temporal and intra-thallus variation in arsenic species in the brown macroalga Laminaria digitata
Rebecca Sim
A B , Joerg Feldmann C , Dagmar B. Stengel D and Ásta H. Pétursdóttir A *
+ Author Affiliations
- Author Affiliations
A Matís, Division of Public Health and Food Safety, Vinlandsleid 12, IS-113 Reykjavík, Iceland.
B Faculty of Physical Sciences, School of Engineering and Natural Sciences, University of Iceland, Dunhagi 3, IS-107, Reykjavík, Iceland.
C TESLA-Analytical Chemistry, Institute for Chemie, University of Graz, Universitätsplatz 1, 8010 Graz, Austria.
D Botany and Plant Science, School of Natural Sciences, University of Galway, University Road, Galway, Ireland.
Environmental Chemistry - https://doi.org/10.1071/EN22123
Submitted: 26 November 2022 Accepted: 10 March 2023 Published online: 4 May 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Environmental context. Arsenic contamination has a disproportionate effect on marine ecosystems. Organisms such as some marine macroalgae, which accumulate potentially toxic elements from the surrounding environment, have developed an internal conversion process that is not yet fully understood. Are arsenic-containing sugars a product of detoxification, or simply the result of phospholipid degradation?
Rationale. Arsenosugars (AsSugar) account for the majority of total arsenic in common seaweed species, yet it is unclear whether these are formed through some detoxification pathway for inorganic arsenic or are precursors/degradation products of arsenic-containing phospholipids in the cell wall.
Methodology. Temporal and intra-thallus variations in water-soluble arsenic were measured by HPLC-ICP-MS, as well as total non-polar and polar arsenic-containing lipids by ICP-MS in Laminaria digitata to offer potential insight into the origins of arsenosugars. Water-soluble speciation with and without freeze-drying were also compared to determine whether freeze-drying changes the water-soluble As speciation.
Results. In general, lower levels of total As were detected in the samples collected in May (39.2–74.5 mg kg−1) compared to those collected in February (72.6–151 mg kg−1). The concentration of arsenate was found to consistently increase along the thallus from the holdfast/stipe (0.78–1.82 mg kg−1) to the decaying fronds (44.4–61.0 mg kg−1) in both months, and AsSug-SO3 was the dominant AsSugar in the majority of samples. The extraction efficiency was lower in fresh samples (64–77%) than in freeze-dried (95–116%) from the same month. Water-soluble, polar AsLipids, and residual As concentrations, were generally highest in February, and the non-polar AsLipids accounted for <0.42% of totAs in all samples.
Discussion. Our results suggest that the arsenosugars are not a product of arsenic detoxification, but a by-product of normal biological activity. It is probable that the arsenosugars are bound to the cell membrane within the Laminaria digitata cells, and lyophilisation is required to release them quantitatively. Future research should focus on speciation of polar lipid-soluble As extracted from fresh samples to determine if the lower extraction efficiency observed in this study is due to the As being in an unextractable form, i.e. lipids, and thus is not removed from cells during water-based extractions.
Keywords: arsenic, arsenic speciation, arsenosugars, inorganic arsenic, macroalgae, seaweed, trace element speciation, trace elements.
References
Al Amin MH, Xiong C, Francesconi KA, et al. (2020). Variation in arsenolipid concentrations in seafood consumed in Japan. Chemosphere 239, 124781| Variation in arsenolipid concentrations in seafood consumed in Japan.Crossref | GoogleScholarGoogle Scholar |
Allahgholi L, Sardari RRR, Hakvåg S, et al. (2020). Composition analysis and minimal treatments to solubilize polysaccharides from the brown seaweed Laminaria digitata for microbial growth of thermophiles. Journal of Applied Phycology 32, 1933–1947.
| Composition analysis and minimal treatments to solubilize polysaccharides from the brown seaweed Laminaria digitata for microbial growth of thermophiles.Crossref | GoogleScholarGoogle Scholar |
Almela C, Jesús Clemente M, Vélez D, et al. (2006). Total arsenic, inorganic arsenic, lead and cadmium contents in edible seaweed sold in Spain. Food and Chemical Toxicology 44, 1901–1908.
| Total arsenic, inorganic arsenic, lead and cadmium contents in edible seaweed sold in Spain.Crossref | GoogleScholarGoogle Scholar |
Amayo KO, Petursdottir A, Newcombe C, et al. (2011). Identification and quantification of arsenolipids using reversed-phase HPLC coupled simultaneously to high-resolution ICPMS and high-resolution electrospray MS without species-specific standards. Analytical Chemistry 83, 3589–3595.
| Identification and quantification of arsenolipids using reversed-phase HPLC coupled simultaneously to high-resolution ICPMS and high-resolution electrospray MS without species-specific standards.Crossref | GoogleScholarGoogle Scholar |
Arroyo-Abad U, Hu Z, Findeisen M, et al. (2016). Synthesis of two new arsenolipids and their identification in fish. European Journal of Lipid Science and Technology 118, 445–452.
| Synthesis of two new arsenolipids and their identification in fish.Crossref | GoogleScholarGoogle Scholar |
Borak J, Hosgood HD (2007). Seafood arsenic: implications for human risk assessment. Regulatory Toxicology and Pharmacology 47, 204–212.
| Seafood arsenic: implications for human risk assessment.Crossref | GoogleScholarGoogle Scholar |
Bruhn A, Janicek T, Manns D, et al. (2017). Crude fucoidan content in two North Atlantic kelp species, Saccharina latissima and Laminaria digitate—seasonal variation and impact of environmental factors. Journal of Applied Phycology 29, 3121–3137.
| Crude fucoidan content in two North Atlantic kelp species, Saccharina latissima and Laminaria digitate—seasonal variation and impact of environmental factors.Crossref | GoogleScholarGoogle Scholar |
Burger J, Gochfeld M, Jeitner C, et al. (2007). Kelp as a Bioindicator: Does it Matter Which Part of 5 M Long Plant is Used for Metal Analysis?. Environmental Monitoring and Assessment 128, 311–321.
| Kelp as a Bioindicator: Does it Matter Which Part of 5 M Long Plant is Used for Metal Analysis?.Crossref | GoogleScholarGoogle Scholar |
CEVA (2019) ‘Edible seaweed and microalgae - Regulatory status in France and Europe.’ (CEVA) Available at https://www.ceva-algues.com/wp-content/uploads/2020/03/CEVA-Edible-algae-FR-and-EU-regulatory-update-2019.pdf
Chen J, Rosen BP (2020). The Arsenic Methylation Cycle: How Microbial Communities Adapted Methylarsenicals for Use as Weapons in the Continuing War for Dominance. Frontiers in Environmental Science 8, 43
| The Arsenic Methylation Cycle: How Microbial Communities Adapted Methylarsenicals for Use as Weapons in the Continuing War for Dominance.Crossref | GoogleScholarGoogle Scholar |
(2002). Directive 2002/32/EC of the European Parliament and of the Council of 7 May 2002 on undesirable substances in animal feed. Official Journal 45, 15
Duncan EG, Maher WA, Foster SD (2015). Contribution of Arsenic Species in Unicellular Algae to the Cycling of Arsenic in Marine Ecosystems. Environmental Science & Technology 49, 33–50.
| Contribution of Arsenic Species in Unicellular Algae to the Cycling of Arsenic in Marine Ecosystems.Crossref | GoogleScholarGoogle Scholar |
Ender E, Subirana MA, Raab A, et al. (2019). Why is NanoSIMS elemental imaging of arsenic in seaweed (Laminaria digitata) important for understanding of arsenic biochemistry in addition to speciation information?. Journal of Analytical Atomic Spectrometry 34, 2295–2302.
| Why is NanoSIMS elemental imaging of arsenic in seaweed (Laminaria digitata) important for understanding of arsenic biochemistry in addition to speciation information?.Crossref | GoogleScholarGoogle Scholar |
Francesconi KA, Edmonds JS, Stick RV, et al. (1991). Arsenic-containing ribosides from the brown alga Sargassum lacerifolium: X-ray molecular structure of 2-amino-3-[5′-deoxy-5′-(dimethylarsinoyl)ribosyloxy]propane-1-sulphonic acid. Journal of the Chemical Society, Perkin Transactions 1, 1991, 2707–2716.
| Arsenic-containing ribosides from the brown alga Sargassum lacerifolium: X-ray molecular structure of 2-amino-3-[5′-deoxy-5′-(dimethylarsinoyl)ribosyloxy]propane-1-sulphonic acid.Crossref | GoogleScholarGoogle Scholar |
Geiszinger A, Goessler W, Pedersen SN, et al. (2001). Arsenic biotransformation by the brown macroalga, Fucus serratus. Environmental Toxicology and Chemistry 20, 2255–2262.
| Arsenic biotransformation by the brown macroalga, Fucus serratus.Crossref | GoogleScholarGoogle Scholar |
Huang Z, Bi R, Musil S, et al. (2022). Arsenic species and their health risks in edible seaweeds collected along the Chinese coastline. Science of the Total Environment 847, 157429
| Arsenic species and their health risks in edible seaweeds collected along the Chinese coastline.Crossref | GoogleScholarGoogle Scholar |
Kim M-h, Kim J, Noh C-H, et al. (2020). Monitoring Arsenic Species Content in Seaweeds Produced off the Southern Coast of Korea and Its Risk Assessment. Environments 7, 68
| Monitoring Arsenic Species Content in Seaweeds Produced off the Southern Coast of Korea and Its Risk Assessment.Crossref | GoogleScholarGoogle Scholar |
Kreissig KJ, Hansen LT, Jensen PE, et al. (2021). Characterisation and chemometric evaluation of 17 elements in ten seaweed species from Greenland. PLoS One 16, e0243672
| Characterisation and chemometric evaluation of 17 elements in ten seaweed species from Greenland.Crossref | GoogleScholarGoogle Scholar |
Lai VW-M, Cullen WR, Harrington CF, Reimer KJ (1998). Seasonal changes in arsenic speciation in Fucus species. Applied Organometallic Chemistry 12, 243–251.
| Seasonal changes in arsenic speciation in Fucus species.Crossref | GoogleScholarGoogle Scholar |
Liu Q, Huang C, Li W, et al. (2021). Discovery and Identification of Arsenolipids Using a Precursor-Finder Strategy and Data-Independent Mass Spectrometry. Environmental Science & Technology 55, 3836–3844.
| Discovery and Identification of Arsenolipids Using a Precursor-Finder Strategy and Data-Independent Mass Spectrometry.Crossref | GoogleScholarGoogle Scholar |
Llorente-Mirandes T, Ruiz-Chancho MJ, Barbero M, et al. (2011). Determination of Water-Soluble Arsenic Compounds in Commercial Edible Seaweed by LC-ICPMS. Journal of Agricultural and Food Chemistry 59, 12963–12968.
| Determination of Water-Soluble Arsenic Compounds in Commercial Edible Seaweed by LC-ICPMS.Crossref | GoogleScholarGoogle Scholar |
Madden M, Mitra M, Ruby D, et al. (2012). Seasonality of selected nutritional constituents of edible Delmarva Seaweeds. Journal of Phycology 48, 1289–1298.
| Seasonality of selected nutritional constituents of edible Delmarva Seaweeds.Crossref | GoogleScholarGoogle Scholar |
Mamun MAA, Omori Y, Papry RI, et al. (2019). Bioaccumulation and biotransformation of arsenic by the brown macroalga Sargassum patens C. Agardh in seawater: effects of phosphate and iron ions. Journal of Applied Phycology 31, 2669–2685.
| Bioaccumulation and biotransformation of arsenic by the brown macroalga Sargassum patens C. Agardh in seawater: effects of phosphate and iron ions.Crossref | GoogleScholarGoogle Scholar |
Matsumoto-Tanibuchi E, Sugimoto T, Kawaguchi T, et al. (2019). Determination of Inorganic Arsenic in Seaweed and Seafood by LC-ICP-MS: Method Validation. Journal of AOAC International 102, 612–618.
| Determination of Inorganic Arsenic in Seaweed and Seafood by LC-ICP-MS: Method Validation.Crossref | GoogleScholarGoogle Scholar |
Meharg AA (2004). Arsenic in rice – understanding a new disaster for South-East Asia. Trends in Plant Science 9, 415–417.
| Arsenic in rice – understanding a new disaster for South-East Asia.Crossref | GoogleScholarGoogle Scholar |
Mitra A, Chatterjee S, Gupta DK (2017) Uptake, Transport, and Remediation of Arsenic by Algae and Higher Plants. In ‘Arsenic Contamination in the Environment: The Issues and Solutions’. (Eds D Gupta, S Chatterjee) pp. 145–169 (Springer International Publishing: Cham)
| Crossref |
Moreda-Piñeiro J, et al. (2016). Determination of Arsenic Species in Edible Seaweeds by HPLC-ICP-MS After Pressurized Hot Water Extraction. Atomic Spectroscopy 37, 218–228.
| Determination of Arsenic Species in Edible Seaweeds by HPLC-ICP-MS After Pressurized Hot Water Extraction.Crossref | GoogleScholarGoogle Scholar |
Narukawa T, Raber G, Itoh N, et al. (2020). A New Candidate Reference Material for Inorganic Arsenic and Arsenosugars in Hijiki Seaweed: First Results from an Inter-laboratory Study. Analytical Sciences 36, 233–237.
| A New Candidate Reference Material for Inorganic Arsenic and Arsenosugars in Hijiki Seaweed: First Results from an Inter-laboratory Study.Crossref | GoogleScholarGoogle Scholar |
Navratilova J, Raber G, Fisher SJ, et al. (2011). Arsenic cycling in marine systems: degradation of arsenosugars to arsenate in decomposing algae, and preliminary evidence for the formation of recalcitrant arsenic. Environmental Chemistry 8, 44–51.
| Arsenic cycling in marine systems: degradation of arsenosugars to arsenate in decomposing algae, and preliminary evidence for the formation of recalcitrant arsenic.Crossref | GoogleScholarGoogle Scholar |
Nearing MM, Koch I, Reimer KJ (2014). Complementary arsenic speciation methods: A review. Spectrochimica Acta Part B: Atomic Spectroscopy 99, 150–162.
| Complementary arsenic speciation methods: A review.Crossref | GoogleScholarGoogle Scholar |
Ometto F, Steinhovden KB, Kuci H, et al. (2018). Seasonal variation of elements composition and biomethane in brown macroalgae. Biomass and Bioenergy 109, 31–38.
| Seasonal variation of elements composition and biomethane in brown macroalgae.Crossref | GoogleScholarGoogle Scholar |
Pengprecha P, Wilson M, Raab A, et al. (2005). Biodegradation of arsenosugars in marine sediment. Applied Organometallic Chemistry 19, 819–826.
| Biodegradation of arsenosugars in marine sediment.Crossref | GoogleScholarGoogle Scholar |
Perini V, Bracken MES (2014). Nitrogen availability limits phosphorus uptake in an intertidal macroalga. Oecologia 175, 667–676.
| Nitrogen availability limits phosphorus uptake in an intertidal macroalga.Crossref | GoogleScholarGoogle Scholar |
Petursdottir AH, Sloth JJ, Feldmann J (2015). Introduction of regulations for arsenic in feed and food with emphasis on inorganic arsenic, and implications for analytical chemistry. Analytical and Bioanalytical Chemistry 407, 8385–8396.
| Introduction of regulations for arsenic in feed and food with emphasis on inorganic arsenic, and implications for analytical chemistry.Crossref | GoogleScholarGoogle Scholar |
Pétursdóttir ÁH, Fletcher K, Gunnlaugsdóttir H, et al. (2016). Environmental effects on arsenosugars and arsenolipids in Ectocarpus (Phaeophyta). Environmental Chemistry 13, 21–33.
| Environmental effects on arsenosugars and arsenolipids in Ectocarpus (Phaeophyta).Crossref | GoogleScholarGoogle Scholar |
Pétursdóttir ÁH, Rodrigues de Jesus J, Gunnlaugsdóttir H, et al. (2018). Quantification of labile and stable non-polar arsenolipids in commercial fish meals and edible seaweed samples. Journal of Analytical Atomic Spectrometry 33, 102–110.
| Quantification of labile and stable non-polar arsenolipids in commercial fish meals and edible seaweed samples.Crossref | GoogleScholarGoogle Scholar |
Pétursdóttir ÁH, Blagden J, Gunnarsson K, et al. (2019). Arsenolipids are not uniformly distributed within two brown macroalgal species Saccharina latissima and Alaria esculenta. Analytical and Bioanalytical Chemistry 411, 4973–4985.
| Arsenolipids are not uniformly distributed within two brown macroalgal species Saccharina latissima and Alaria esculenta.Crossref | GoogleScholarGoogle Scholar |
Rahman MA, Hasegawa H, Ueda K, et al. (2008). ) Influence of phosphate and iron ions in selective uptake of arsenic species by water fern (Salvinia natans L.). Chemical Engineering Journal 145, 179–184.
| ) Influence of phosphate and iron ions in selective uptake of arsenic species by water fern (Salvinia natans L.).Crossref | GoogleScholarGoogle Scholar |
Roleda MY, Hurd CL (2019). Seaweed nutrient physiology: application of concepts to aquaculture and bioremediation. Phycologia 58, 552–562.
| Seaweed nutrient physiology: application of concepts to aquaculture and bioremediation.Crossref | GoogleScholarGoogle Scholar |
Ronan JM, Stengel DB, Raab A, et al. (2017). High proportions of inorganic arsenic in Laminaria digitata but not in Ascophyllum nodosum samples from Ireland. Chemosphere 186, 17–23.
| High proportions of inorganic arsenic in Laminaria digitata but not in Ascophyllum nodosum samples from Ireland.Crossref | GoogleScholarGoogle Scholar |
Rubio R, Ruiz-Chancho MJ, López-Sánchez JF, et al. (2010). Sample pre-treatment and extraction methods that are crucial to arsenic speciation in algae and aquatic plants. TrAC Trends in Analytical Chemistry 29, 53–69.
| Sample pre-treatment and extraction methods that are crucial to arsenic speciation in algae and aquatic plants.Crossref | GoogleScholarGoogle Scholar |
Schmid M, Guihéneuf F, Stengel DB (2017). Ecological and commercial implications of temporal and spatial variability in the composition of pigments and fatty acids in five Irish macroalgae. Marine Biology 164, 158
| Ecological and commercial implications of temporal and spatial variability in the composition of pigments and fatty acids in five Irish macroalgae.Crossref | GoogleScholarGoogle Scholar |
Shen S, Li X-F, Cullen WR, et al. (2013). Arsenic binding to proteins. Chemical Reviews 113, 7769–7792.
| Arsenic binding to proteins.Crossref | GoogleScholarGoogle Scholar |
Stengel DB, McGrath H, Morrison LJ (2005). Tissue Cu, Fe and Mn concentrations in different-aged and different functional thallus regions of three brown algae from western Ireland. Estuarine, Coastal and Shelf Science 65, 687–696.
| Tissue Cu, Fe and Mn concentrations in different-aged and different functional thallus regions of three brown algae from western Ireland.Crossref | GoogleScholarGoogle 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.
| Concentrations and speciation of arsenic in New England seaweed species harvested for food and agriculture.Crossref | GoogleScholarGoogle Scholar |
Tibon J, Silva M, Sloth JJ, et al. (2021). Speciation analysis of organoarsenic species in marine samples: method optimization using fractional factorial design and method validation. Analytical and Bioanalytical Chemistry 413, 3909–3923.
| Speciation analysis of organoarsenic species in marine samples: method optimization using fractional factorial design and method validation.Crossref | GoogleScholarGoogle Scholar |
Wang Y, Wang S, Xu P, et al. (2015). Review of arsenic speciation, toxicity and metabolism in microalgae. Reviews in Environmental Science and Bio/Technology 14, 427–451.
| Review of arsenic speciation, toxicity and metabolism in microalgae.Crossref | GoogleScholarGoogle Scholar |
Wolle MM, Conklin SD (2018). Speciation analysis of arsenic in seafood and seaweed: Part I—evaluation and optimization of methods. Analytical and Bioanalytical Chemistry 410, 5675–5687.
| Speciation analysis of arsenic in seafood and seaweed: Part I—evaluation and optimization of methods.Crossref | GoogleScholarGoogle Scholar |
Xue X-M, Ye J, Raber G, et al. (2017). Arsenic Methyltransferase is Involved in Arsenosugar Biosynthesis by Providing DMA. Environmental Science & Technology 51, 1224–1230.
| Arsenic Methyltransferase is Involved in Arsenosugar Biosynthesis by Providing DMA.Crossref | GoogleScholarGoogle Scholar |
Xue X-M, Ye J, Raber G, et al. (2019). Identification of Steps in the Pathway of Arsenosugar Biosynthesis. Environmental Science & Technology 53, 634–641.
| Identification of Steps in the Pathway of Arsenosugar Biosynthesis.Crossref | GoogleScholarGoogle Scholar |
