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Environmental problems - Chemical approaches
RESEARCH ARTICLE

Lipids that contain arsenic in the Mediterranean mussel, Mytilus galloprovincialis

Fabiana P. Freitas https://orcid.org/0000-0003-0280-2181 A C , Georg Raber B , Kenneth B. Jensen B , António J. A. Nogueira A and Kevin A. Francesconi B
+ Author Affiliations
- Author Affiliations

A Department of Biology and CESAM, University of Aveiro, 3810 Aveiro, Portugal.

B Institute of Chemistry, University of Graz, Universitaetsplatz 1, 8010 Graz, Austria.

C Corresponding author. Email: fabiana@ua.pt

Environmental Chemistry 17(3) 289-301 https://doi.org/10.1071/EN19213
Submitted: 31 July 2019  Accepted: 2 October 2019   Published: 18 December 2019

Environmental context. Although arsenic-containing lipids are widespread in marine environments, their origin remains unknown. We show that the arsenolipids in a filter-feeding bivalve mollusc closely match those found in marine food sources, including unicellular algae and bacteria. The results demonstrate the role of lower trophic levels in determining the forms of arsenic found in higher organisms.

Abstract. Arsenic-containing lipids, arsenolipids, are widely found among marine organisms, but their origin and possible biochemical roles remain unknown This work describes the diversity and abundance of arsenolipids in the digestive gland and mantle of nine specimens of the Mediterranean mussel, Mytilus galloprovincialis. By using high performance liquid chromatography (HPLC) coupled to both elemental and high-resolution molecular mass spectrometry, we identified 36 arsenolipids including arsenic derivatives of fatty acids, hydrocarbons, sugar-phospholipids and sugar-phytol; 21 of these arsenolipids were identified for the first time and included a new group comprising ether-phospholipids. The arsenic compounds in the mussels show distinct profiles depending on the tissue type, which provide insight into the arsenolipid origin. The results suggest that the presence of some arsenolipids in the mussels is from direct uptake of the compounds, presumably from food, rather than biogenesis within the mussels.


References

Ackman RG, Eaton CA, Dyerberg J (1980a). Marine docosenoic acid isomer distribution in the plasma of Greenland Eskimos. The American Journal of Clinical Nutrition 33, 1814–1817.
Marine docosenoic acid isomer distribution in the plasma of Greenland EskimosCrossref | GoogleScholarGoogle Scholar |

Ackman RG, Sebedio JL, Kovacs MIP (1980b). Role of eicosenoic and docosenoic fatty acids in fresh water and marine lipids. Marine Chemistry 9, 157–164.
Role of eicosenoic and docosenoic fatty acids in fresh water and marine lipidsCrossref | GoogleScholarGoogle Scholar |

Amayo KO, Petursdottir A, Newcombe C, Gunnlaugsdottir H, Raab A, Krupp EM, Feldmann J (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 standardsCrossref | GoogleScholarGoogle Scholar | 21446761PubMed |

Amayo KO, Raab A, Krupp EM, Gunnlaugsdottir H, Feldmann J (2013). Novel identification of arsenolipids using chemical derivatizations in conjunction with RP-HPLC-ICPMS/ESMS. Analytical Chemistry 85, 9321–9327.
Novel identification of arsenolipids using chemical derivatizations in conjunction with RP-HPLC-ICPMS/ESMSCrossref | GoogleScholarGoogle Scholar | 23984920PubMed |

Arroyo-Abad U, Lischka S, Piechotta C, Mattusch J, Reemtsma T (2013). Determination and identification of hydrophilic and hydrophobic arsenic species in methanol extract of fresh cod liver by RP-HPLC with simultaneous ICP-MS and ESI-Q-TOF-MS detection. Food Chemistry 141, 3093–3102.
Determination and identification of hydrophilic and hydrophobic arsenic species in methanol extract of fresh cod liver by RP-HPLC with simultaneous ICP-MS and ESI-Q-TOF-MS detectionCrossref | GoogleScholarGoogle Scholar | 23871064PubMed |

Arroyo-Abad U, Hu Z, Findeisen M, Pfeifer D, Mattusch J, Reemtsma T, Piechotta C (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 fishCrossref | GoogleScholarGoogle Scholar |

Byelashov OA, Sinclair AJ, Kaur G (2015). Dietary sources, current intakes, and nutritional role of omega-3 docosapentaenoic acid. Lipid Technology 27, 79–82.
Dietary sources, current intakes, and nutritional role of omega-3 docosapentaenoic acidCrossref | GoogleScholarGoogle Scholar | 26097290PubMed |

Cequier-Sánchez E, Rodríguez C, Ravelo ÁG, Zárate R (2008). Dichloromethane as a solvent for lipid extraction and assessment of lipid classes and fatty acids from samples of different natures. Journal of Agricultural and Food Chemistry 56, 4297–4303.
Dichloromethane as a solvent for lipid extraction and assessment of lipid classes and fatty acids from samples of different naturesCrossref | GoogleScholarGoogle Scholar | 18505264PubMed |

Conway N, McDowell Capuzzo J (1991). Incorporation and utilization of bacterial lipids in the Solemya velum symbiosis. Marine Biology 108, 277–291.
Incorporation and utilization of bacterial lipids in the Solemya velum symbiosisCrossref | GoogleScholarGoogle Scholar |

Dean JM, Lodhi IJ (2018). Structural and functional roles of ether lipids. Protein & Cell 9, 196–206.
Structural and functional roles of ether lipidsCrossref | GoogleScholarGoogle Scholar |

Dernekbaşı S (2015). The fatty acid composition of cultured mussels (Mytilus galloprovincialis Lamarck 1819) in offshore longline system in the Black Sea. Journal of Aquaculture & Marine Biology 2, 00049
The fatty acid composition of cultured mussels (Mytilus galloprovincialis Lamarck 1819) in offshore longline system in the Black SeaCrossref | GoogleScholarGoogle Scholar |

El Ashry ESH, Atta-ur-Rahman , Choudhary MI, Kandil SH, El Nemr A, Gulzar T, Shobier AH (2011). Studies on the constituents of the green alga Ulva lactuca. Chemistry of Natural Compounds 47, 335–338.
Studies on the constituents of the green alga Ulva lactucaCrossref | GoogleScholarGoogle Scholar |

Farrington JW, Tripp BW (1995). International Mussel Watch Project: initial implementation phase, final report. NOAA Technical Memorandum. U.S. Dept. of Commerce, National Oceanic and Atmospheric Administration, National Ocean Service, Office of Ocean Resources Conservation and Assessment, Silver Spring, MD10.5962/BHL.TITLE.4173

Fearman J-A, Bolch CJS, Moltschaniwskyj NA (2009). Energy storage and reproduction in mussels, Mytilus galloprovincialis: The influence of diet quality. Journal of Shellfish Research 28, 305–312.
Energy storage and reproduction in mussels, Mytilus galloprovincialis: The influence of diet qualityCrossref | GoogleScholarGoogle Scholar |

García-Salgado S, Raber G, Raml R, Magnes C, Francesconi KA (2012). Arsenosugar phospholipids and arsenic hydrocarbons in two species of brown macroalgae. Environmental Chemistry 9, 63–66.
Arsenosugar phospholipids and arsenic hydrocarbons in two species of brown macroalgaeCrossref | GoogleScholarGoogle Scholar |

George EM, Parrish CC (2015). Invertebrate uptake of lipids in the vicinity of Atlantic salmon (Salmo salar) aquaculture sites in British Columbia. Aquaculture Research 46, 1044–1065.
Invertebrate uptake of lipids in the vicinity of Atlantic salmon (Salmo salar) aquaculture sites in British ColumbiaCrossref | GoogleScholarGoogle Scholar |

Glabonjat RA, Raber G, Jensen KB, Ehgartner J, Francesconi KA (2014). Quantification of arsenolipids in the certified reference material NMIJ 7405-a (Hijiki) using HPLC/mass spectrometry after chemical derivatization. Analytical Chemistry 86, 10282–10287.
Quantification of arsenolipids in the certified reference material NMIJ 7405-a (Hijiki) using HPLC/mass spectrometry after chemical derivatizationCrossref | GoogleScholarGoogle Scholar | 25241916PubMed |

Glabonjat RA, Raber G, Jensen KB, Guttenberger N, Zangger K, Francesconi KA (2017). A 2-O-Methylriboside Unknown Outside the RNA World Contains Arsenic. Angewandte Chemie 129, 12125–12127.
A 2-O-Methylriboside Unknown Outside the RNA World Contains ArsenicCrossref | GoogleScholarGoogle Scholar |

Jamieson T, Wardlaw AC (1989). Degradation of bacterial lipopolysaccharides by digestive-gland extracts of marine bivalve molluscs. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 94, 837–843.
Degradation of bacterial lipopolysaccharides by digestive-gland extracts of marine bivalve molluscsCrossref | GoogleScholarGoogle Scholar |

Kaur G, Cameron-Smith D, Garg M, Sinclair AJ (2011). Docosapentaenoic acid (22:5n-3): A review of its biological effects. Progress in Lipid Research
Docosapentaenoic acid (22:5n-3): A review of its biological effectsCrossref | GoogleScholarGoogle Scholar | 20655949PubMed |

Lischka S, Arroyo-Abad U, Mattusch J, Kühn A, Piechotta C (2013). The high diversity of arsenolipids in herring fillet (Clupea harengus). Talanta 110, 144–152.
The high diversity of arsenolipids in herring fillet (Clupea harengus)Crossref | GoogleScholarGoogle Scholar | 23618187PubMed |

Martínez-Pita I, Sánchez-Lazo C, Ruíz-Jarabo I, Herrera M, Mancera JM (2012). Biochemical composition, lipid classes, fatty acids and sexual hormones in the mussel Mytilus galloprovincialis from cultivated populations in south Spain. Aquaculture 358–359, 274–283.
Biochemical composition, lipid classes, fatty acids and sexual hormones in the mussel Mytilus galloprovincialis from cultivated populations in south SpainCrossref | GoogleScholarGoogle Scholar |

Matyash V, Liebisch G, Kurzchalia TV, Shevchenko A, Schwudke D (2008). Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. Journal of Lipid Research 49, 1137–1146.
Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomicsCrossref | GoogleScholarGoogle Scholar | 18281723PubMed |

Meyer S, Matissek M, Müller SM, Taleshi MS, Ebert F, Francesconi KA, Schwerdtle T (2014a). In vitro toxicological characterisation of three arsenic-containing hydrocarbons. Metallomics 6, 1023–1033.
In vitro toxicological characterisation of three arsenic-containing hydrocarbonsCrossref | GoogleScholarGoogle Scholar | 24718560PubMed |

Meyer S, Schulz J, Jeibmann A, Taleshi MS, Ebert F, Francesconi KA, Schwerdtle T (2014b). Arsenic-containing hydrocarbons are toxic in the in vivo model Drosophila melanogaster. Metallomics 6, 2010–2014.
Arsenic-containing hydrocarbons are toxic in the in vivo model Drosophila melanogasterCrossref | GoogleScholarGoogle Scholar | 25292248PubMed |

Mishra PM, Sree A (2009). Fatty acid profile, volatiles and antibacterial screening of lipids of the sponge Siphonodictyon coralliphagum collected from the Bay of Bengal (Orissa Coast). Journal of the Serbian Chemical Society 21, 4429–4434.
Fatty acid profile, volatiles and antibacterial screening of lipids of the sponge Siphonodictyon coralliphagum collected from the Bay of Bengal (Orissa Coast)Crossref | GoogleScholarGoogle Scholar |

Morita M, Shibata Y (1988). Isolation and identification of arseno-lipid from a brown alga, Undaria pinnatifida (Wakame). Chemosphere
Isolation and identification of arseno-lipid from a brown alga, Undaria pinnatifida (Wakame)Crossref | GoogleScholarGoogle Scholar |

Nagan N, Zoeller RA (2001). Plasmalogens: biosynthesis and functions. Progress in Lipid Research 40, 199–229.
Plasmalogens: biosynthesis and functionsCrossref | GoogleScholarGoogle Scholar | 11275267PubMed |

Niehoff A-C, Schulz J, Soltwisch J, Meyer S, Kettling H, Sperling M, Jeibmann A, Dreisewerd K, Francesconi KA, Schwerdtle T, Karst U (2016). Imaging by Elemental and Molecular Mass Spectrometry Reveals the Uptake of an Arsenolipid in the Brain of Drosophila melanogaster. Analytical Chemistry 88, 5258–5263.
Imaging by Elemental and Molecular Mass Spectrometry Reveals the Uptake of an Arsenolipid in the Brain of Drosophila melanogasterCrossref | GoogleScholarGoogle Scholar | 27098356PubMed |

Parrish CC (2013). Lipids in Marine Ecosystems. ISRN Oceanography 2013, 1–16.
Lipids in Marine EcosystemsCrossref | GoogleScholarGoogle Scholar |

Pereira ÉR, Kopp JF, Raab A, Krupp EM, Menoyo J del C, Carasek E, Welz B, Feldmann J (2016). Arsenic containing medium and long chain fatty acids in marine fish oil identified as degradation products using reversed-phase HPLC-ICP-MS/ESI-MS. Journal of Analytical Atomic Spectrometry 31, 1836–1845.
Arsenic containing medium and long chain fatty acids in marine fish oil identified as degradation products using reversed-phase HPLC-ICP-MS/ESI-MSCrossref | GoogleScholarGoogle Scholar |

Perry GJ, Volkman JK, Johns RB, Bavor HJ (1979). Fatty acids of bacterial origin in contemporary marine sediments. Geochimica et Cosmochimica Acta 43, 1715–1725.
Fatty acids of bacterial origin in contemporary marine sedimentsCrossref | GoogleScholarGoogle Scholar |

Raab A, Newcombe C, Pitton D, Ebel R, Feldmann J (2013). Comprehensive analysis of lipophilic arsenic species in a brown alga (Saccharina latissima). Analytical Chemistry 85, 2817–2824.
Comprehensive analysis of lipophilic arsenic species in a brown alga (Saccharina latissima)Crossref | GoogleScholarGoogle Scholar | 23394220PubMed |

Raber G, Raml R, Goessler W, Francesconi KA (2010). Quantitative speciation of arsenic compounds when using organic solvent gradients in HPLC-ICPMS. Journal of Analytical Atomic Spectrometry 25, 570–576.
Quantitative speciation of arsenic compounds when using organic solvent gradients in HPLC-ICPMSCrossref | GoogleScholarGoogle Scholar |

Řezanka T, Sigler K (2009). Odd-numbered very-long-chain fatty acids from the microbial, animal and plant kingdoms. Progress in Lipid Research 48, 206–238.
Odd-numbered very-long-chain fatty acids from the microbial, animal and plant kingdomsCrossref | GoogleScholarGoogle Scholar | 19336244PubMed |

Řezanka T, Nedbalová L, Barcytė D, Vítová M, Sigler K (2019). Arsenolipids in the green alga Coccomyxa (Trebouxiophyceae, Chlorophyta). Phytochemistry
Arsenolipids in the green alga Coccomyxa (Trebouxiophyceae, Chlorophyta)Crossref | GoogleScholarGoogle Scholar | 31128818PubMed |

Rodríguez F, Feist SW, Guillou L, Harkestad LS, Bateman K, Renault T, Mortensen S, Rodriguez F, Feist SW, Guillou L, Harkestad LS, Bateman K, Renault T, Mortensen S (2008). Phylogenetic and morphological characterisation of the green algae infesting blue mussel Mytilus edulis in the North and South Atlantic oceans. Diseases of Aquatic Organisms 81, 231–240.
Phylogenetic and morphological characterisation of the green algae infesting blue mussel Mytilus edulis in the North and South Atlantic oceansCrossref | GoogleScholarGoogle Scholar | 18998587PubMed |

Rodriguez y Baena AM, Thébault H (2006). CIESM Mediterranean Mussel Watch Program Phase II: towards an increased awareness of marine environment and seafood quality. In ‘Marine sciences and public health – some major issues’. CIESM Workshop Monograph No. 31 (Ed. F Briand) pp. 87–89. (CIESM Publisher: Monaco)

Rumpler A, Edmonds JS, Katsu M, Jensen KB, Goessler W, Raber G, Gunnlaugsdottir H, Francesconi KA (2008). Arsenic-containing Long-chain fatty acids in cod-liver oil: A result of biosynthetic infidelity?. Angewandte Chemie International Edition 47, 2665–2667.
Arsenic-containing Long-chain fatty acids in cod-liver oil: A result of biosynthetic infidelity?Crossref | GoogleScholarGoogle Scholar | 18306198PubMed |

Sadolin E (1928). Untersuchungen über das Vorkommen des Arsens im Organismus der Fische. Biochemische Zeitschrift 201, 323–331.

Tabarsa M, Rezaei M, Ramezanpour Z, Waaland JR (2012). Chemical compositions of the marine algae Gracilaria salicornia (Rhodophyta) and Ulva lactuca (Chlorophyta) as a potential food source. Journal of the Science of Food and Agriculture 92, 2500–2506.
Chemical compositions of the marine algae Gracilaria salicornia (Rhodophyta) and Ulva lactuca (Chlorophyta) as a potential food sourceCrossref | GoogleScholarGoogle Scholar | 22467477PubMed |

Taleshi MS, Jensen KB, Raber G, Edmonds JS, Gunnlaugsdottir H, Francesconi KA (2008). Arsenic-containing hydrocarbons: natural compounds in oil from the fish capelin, Mallotus villosus. Chemical Communications 39, 4706–4707.
Arsenic-containing hydrocarbons: natural compounds in oil from the fish capelin, Mallotus villosusCrossref | GoogleScholarGoogle Scholar |

Taleshi MS, Raber G, Edmonds JS, Jensen KB, Francesconi KA (2014a). Arsenolipids in oil from blue whiting Micromesistius poutassou - Evidence for arsenic-containing esters. Scientific Reports 4, 7492
Arsenolipids in oil from blue whiting Micromesistius poutassou - Evidence for arsenic-containing estersCrossref | GoogleScholarGoogle Scholar | 25502848PubMed |

Taleshi MS, Seidler-Egdal RK, Jensen KB, Schwerdtle T, Francesconi KA (2014b). Synthesis and characterization of arsenolipids: Naturally occurring arsenic compounds in fish and algae. Organometallics 33, 1397–1403.
Synthesis and characterization of arsenolipids: Naturally occurring arsenic compounds in fish and algaeCrossref | GoogleScholarGoogle Scholar | 24683287PubMed |

Taylor V, Goodale B, Raab A, Schwerdtle T, Reimer K, Conklin S, Karagas MR, Francesconi KA (2017). Human exposure to organic arsenic species from seafood. The Science of the Total Environment 580, 266–282.
Human exposure to organic arsenic species from seafoodCrossref | GoogleScholarGoogle Scholar | 28024743PubMed |

Viczek SA, Jensen KB, Francesconi KA (2016). Arsenic-containing phosphatidylcholines: a new group of arsenolipids discovered in Herring caviar. Angewandte Chemie International Edition 55, 5259–5262.
Arsenic-containing phosphatidylcholines: a new group of arsenolipids discovered in Herring caviarCrossref | GoogleScholarGoogle Scholar | 26996517PubMed |

Williams PM (1965). Fatty acids derived from lipids of marine origin. Journal of the Fisheries Research Board of Canada 22, 1107–1122.
Fatty acids derived from lipids of marine originCrossref | GoogleScholarGoogle Scholar |

Yu X, Xiong C, Jensen KB, Glabonjat RA, Stiboller M, Raber G, Francesconi KA (2018). Mono-acyl arsenosugar phospholipids in the edible brown alga Kombu (Saccharina japonica). Food Chemistry
Mono-acyl arsenosugar phospholipids in the edible brown alga Kombu (Saccharina japonica)Crossref | GoogleScholarGoogle Scholar | 30724212PubMed |