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King's Research Portal King’s Research Portal DOI: 10.1039/C8MT00078F Document Version Peer reviewed version Link to publication record in King's Research Portal Citation for published version (APA): Thompson, E. D., Hogstrand, C., & Glover, C. N. (2018). From sea squirts to squirrelfish: facultative trace element hyperaccumulation in animals. Metallomics. https://doi.org/10.1039/C8MT00078F Citing this paper Please note that where the full-text provided on King's Research Portal is the Author Accepted Manuscript or Post-Print version this may differ from the final Published version. If citing, it is advised that you check and use the publisher's definitive version for pagination, volume/issue, and date of publication details. And where the final published version is provided on the Research Portal, if citing you are again advised to check the publisher's website for any subsequent corrections. 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Sep. 2021 Metallomics From sea squirts to squirrelfish: facultative trace element hyperaccumulation in animals Journal: Metallomics Manuscript ID MT-CRV-04-2018-000078.R2 Article Type: Critical Review Date Submitted by the Author: 21-May-2018 Complete List of Authors: Thompson, David; Northern Kentucky University, Hogstrand, Christer; King’s College London, Diabetes and Nutritional Sciences, School of Medicine Glover, Chris; Athabasca University Page 1 of 51 Metallomics 1 2 3 1 From sea squirts to squirrelfish: facultative trace element 4 5 2 6 hyperaccumulation in animals 7 8 3 9 10 4 E. David Thompson1,*, Christer Hogstrand2, Chris N. Glover3,4 11 12 13 5 14 1 15 6 Department of Biological Sciences, Northern Kentucky University, USA 16 2 17 7 Faculty of Life Sciences and Medicine, King’s College London, UK 18 19 8 3Faculty of Science and Technology and Athabasca River Basin Research Institute, 20 21 9 Athabasca University, Canada 22 23 10 4Department of Biological Sciences, University of Alberta, Canada 24 25 11 26 27 28 12 29 30 13 * Corresponding author at: 31 32 14 SC 245 Nunn Dr 33 34 15 Highland Heights, KY 41099 35 36 16 Email: [email protected] 37 38 17 39 40 41 18 42 43 19 44 45 20 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Metallomics Page 2 of 51 1 2 3 21 Abstract 4 5 22 6 7 23 The hyperaccumulation of trace elements is a widely characterized phenomenon in 8 9 24 plants, bacteria, and fungi, but has received little attention in animals. However, there are 10 11 25 numerous examples of animals that specifically and facultatively accumulate trace elements 12 13 14 26 in the absence of elevated environmental concentrations. Metal hyperaccumulating animals 15 16 27 are usually marine invertebrates, likely owing to environmental (e.g. constant exposure via 17 18 28 the water) and physiological (e.g. osmoconforming and reduced integument permeability) 19 20 29 factors. However, there are examples of terrestrial animals (insect larvae) and marine 21 22 30 vertebrates (e.g. squirrelfish) that accumulate high body and/or tissue metal burdens. This 23 24 31 review examines examples of animal hyperaccumulation of the elements arsenic, copper, 25 26 27 32 iron, titanium, vanadium and zinc, describing mechanisms by which accumulation occurs 28 29 33 and, where possible, hypothesizing functional roles. Groups such as the ascidians (sea 30 31 34 squirts), molluscs (gastropods, bivalves and cephalopods) and polychaete annelids feature 32 33 35 prominently as animals with hyperaccumulating capacity. Many of these species are potential 34 35 36 model organisms offering insight into fundamental processes underlying metal handling, with 36 37 37 relevance to human disease and aquatic metal toxicity, and some offer promise in applied 38 39 40 38 fields such as bioremediation. 41 42 39 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Page 3 of 51 Metallomics 1 2 3 40 Significance to metallomics 4 5 41 6 7 42 This review examines examples of hyperaccumulation in animals, the mechanisms by 8 9 43 which this is achieved, the biological roles that have been proposed for this phenomenon, and 10 11 44 identifies knowledge gaps requiring further research. The hyperaccumulation of trace metals 12 13 14 45 such as arsenic, copper, iron, titanium, vanadium and zinc in animal models can offer 15 16 46 significant insight into human metal handling disorders and the risks associated with 17 18 47 environmental metal contamination. 19 20 48 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Metallomics Page 4 of 51 1 2 3 49 Introduction 4 5 50 6 7 51 Trace elements are those that are found at relatively low concentrations within the 8 9 52 environment, and biologically can be classified as either essential or non-essential. Essential 10 11 53 elements such as copper (Cu), zinc (Zn), and iron (Fe) perform a variety of key functions 12 13 1 14 54 through their association with biomolecules such as proteins. However, even elements that in 15 16 55 human biology are considered non-essential, for example the metalloid arsenic (As), still can 17 18 56 have important roles in other biota.2 For most elements, and in most organisms, accumulation 19 20 57 is limited, usually through regulation of uptake and/or excretion.1 This is vital as even 21 22 58 essential elements accumulated to high concentrations can cause a variety of deleterious 23 24 59 effects. However, there are a number of species that maintain elevated concentrations of 25 26 27 60 elements within specific tissues and/or cellular compartments. This is a particularly 28 29 61 prominent phenomenon in plants, wherein approximately 500 taxa can be defined as metal 30 31 62 hyperaccumulators.3-6 While hyperaccumulation has also been widely noted in bacteria, 32 33 63 yeast, and fungi,7,8 it has received little attention in animals. This is somewhat surprising 34 35 64 given the potential importance of animal hyperaccumulators as model species for 36 37 65 understanding processes critical for ecological risk assessment (e.g. regulatory tools utilizing 38 39 9,10 11 12 40 66 body burden as a predictor of impact), environmental remediation, food safety, and 41 13 42 67 human disease. To address this gap, the current review seeks to summarize the existing 43 44 68 literature regarding facultative trace element hyperaccumulation in animals, particularly 45 46 69 focussing on trace metals and metalloids. 47 48 70 49 50 71 Hyperaccumulation: defined and refined 51 52 72 53 54 55 56 57 58 59 60 Page 5 of 51 Metallomics 1 2 3 73 In the current review, we define hyperaccumulators as species that concentrate 4 5 74 elements to levels greater than 1 000 mg kg-1, on either a whole animal or tissue basis. To 6 7 75 place this threshold in context, Luoma and Rainbow conducted a literature survey of 8 9 76 bioaccumulation in aquatic organisms, including those from contaminated ecosystems, and 10 11 77 found that 88% of trace element concentrations fell between 0.1 and 100 mg kg-1.14 It is 12 13 14 78 important to highlight that our definition of hyperaccumulation is simplified relative to that 15 11 16 79 used by previous authors, in that it uses the same threshold for all trace elements, rather 17 18 80 than making element-specific distinction. Consistent with some definitions of 19 20 81 hyperaccumulation in the plant literature,15 we largely exclude from discussion those animals 21 22 82 in which experimental exposures can result in increased tissue element burdens, and also 23 24 83 those animals exposed naturally to extreme environmental contamination scenarios. 25 26 27 84 Consequently, we focus on facultative hyperaccumulators. These are animals that 28 29 85 strategically concentrate elements, without evidence of a toxicological impact, and in spite of 30 31 86 relatively low environmental concentrations. It is notable that for many of these species the 32 33 87 functional role of hyperaccumulation has yet to be discerned. 34 35 88 In some studies hyperaccumulation can be a consequence of how animals or tissues 36 37 89 are handled for analysis. For example, failure to flush or depurate gut contents can result in 38 39 40 90 artificially elevated tissue burdens by measuring gastrointestinal sediments or prey items that 41 16 42 91 may have elevated metal contents, but which are not accumulated. This will be particularly 43 44 92 important where there is an unrecognized environmental enrichment of elements (e.g. 45 46 93 contamination and/or metal-enriched geology). An example of this effect is in studies of Fe 47 48 94 accumulation in field-collected ascidians, where it was noted that body burdens reduced 49 50 95 significantly after animals were held in clean seawater for several days following collection.17 51 52 96 53 This was attributed to the flushing of Fe-containing particulate matter originating from the 54 55 97 point of collection, from the body cavity.
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