Metal Compartmentalization Research Articles

Distribution of micro-essential (Fe, Cu, Zn) and toxic (Hg) metals in tissues of two nutritionally distinct hydrothermal shrimps

Hydrothermal ecosystems of the Mid Atlantic Ridge (MAR) are dominated by shrimps and mussels that are naturally exposed to elevated levels of heavy metals providing unique in situ laboratories for ecotoxicological investigations. This study reports on the tissue compartmentalization of both micro-essential (Fe, Zn, Cu) and toxic metals (Hg) in two nutritionally distinct cariddean vent shrimps: Rimicaris exoculata and Mirocaris fortunata, in order to shed light on organism–biota interactions at hydrothermal vents. High metal concentrations in shrimps confirmed extreme exposure levels at both geochemically different hydrothermal vents (Rainbow and Lucky Strike). However, Hg concentrations were below those reported in species for human consumption that may either suggest low bioavailability of the metal, or its effective detoxification/depuration by the hydrothermal shrimp that needs to be confirmed by post-capture toxicological investigations. Distribution of metals in different tissues had very similar patterns in both shrimp species, the target organs being gill and pylorus. Tissue levels correlated well with end-member fluid composition with regard to element ratios, i.e. Fe / Zn and Fe / Cu ratios in end-member fluids reported for Rainbow and L. Strike were conserved in the gills of M. fortunata. Moreover, R. exoculata that lives closer to venting exits as compared to M. fortunata, had similar or often less metals accumulated in selected organs, possibly owing to its higher degree of adaptation to hydrothermal conditions. Despite of high concentrations in tissues micro essential metals only represented a small fraction (14–36%) of the whole body burden indicating preponderance of minerals on the surface and/or in the gut, and thus points to improper use of whole body concentration in metal bioavailability interpretations at hydrothermal vents.

Biological factors influencing tissue compartmentalization of trace metals in the deep-sea hydrothermal vent bivalve Bathymodiolus azoricus at geochemically distinct vent sites of the Mid-Atlantic Ridge

In this study, we investigated on concentrations of trace metals (Al, Cd, Mn, Co, and Hg) in the hydrothermal bivalve Bathymodiolus azoricus, a dominant species at most vent sites along the Mid-Atlantic Ridge (MAR), and in its endosymbiont bacteria and commensal parasite Branchipolynoe seepensis. Comparison of our results with data from the literature on nonhydrothermal bivalves suggests lack of “extreme” uptake of trace metals by B. azoricus, except for Hg concentration which exceeded manyfold previously reported values. Mussels collected from three geochemically distinct vent sites, Menez Gwen, Lucky Strike, and Rainbow, along the MAR showed significant differences in tissue concentration of metals. Proportionality of metals in soft tissues of mussels reflected variation of water chemistry at different vents, which in turn conserved the order of trace metal prevalence in undiluted fluids. There were significant tissue-specific differences in trace metal compartmentalization for all metals investigated. Byssus thread contained the highest metal concentration among examined tissues, and thus it is suggested to be an important detoxification route. Size-dependent differences in metal concentrations were detected only for Hg, revealing a general trend of small mussels accumulating more metal than big mussels. Endosymbiont bacteria are shown to exclusively sequester Al from the host gill and contribute to removal of other toxic metals in mussels from Menez Gwen. The commensal parasite present in all mussels from Lucky Strike had higher tissue concentrations of Mn, Al, and Co than the host gill, unlike Cd and Hg which were considerably lower in the former, and thus its role in detoxification remains unclear. Bioaccumulation potential of vent bivalves and associated organisms are quantified as concentration factors and compared to make inferences on the putative role of the endosymbiont bacteria and the commensal parasite in detoxification of trace metals.

Application of Quantitative Fluorescence and Absorption-Edge Computed Microtomography to Image Metal Compartmentalization in Alyssum murale

This paper shows that synchrotron-based fluorescence and absorption-edge computed microtomographies (CMT) are well-suited for determining the compartmentalization and concentration of metals in hyperaccumulating plant tissues. Fluorescence CMT of intact leaf, stem, and root samples revealed that Ni concentrated in stem and leaf dermal tissues and, together with Mn, in distinct regions associated with the Ca-rich trichomes on the leaf surface of the nickel hyperaccumulator Alyssum murale "Kotodesh". Metal enrichment was also observed within the vascular system of the finer roots, stem, and leaves but absent from the coarser root, which had a well-correlated metal coating. Absorption-edge CMT showed the three-dimensional distribution of the highest metal concentrations and verified that epidermal localization and Ni and Mn co-localization at the trichome base are phenomena that occurred throughout the entire leaf and may contribute significantly to metal detoxification and storage. Ni was also observed in the leaf tips, possibly resulting from release of excess Ni with guttation fluids. These results are consistent with a transport model where Ni is removed from the soil by the finer roots, carried to the leaves through the stem xylem, and distributed throughout the leaf by the veins to the dermal tissues, trichome bases, and in some cases the leaf tips.

Influence of subcellular metal compartmentalization in different prey on the transfer of metals to a predatory gastropod

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 286:155-166 (2005) - doi:10.3354/meps286155 Influence of subcellular metal compartmentalization in different prey on the transfer of metals to a predatory gastropod Mashan Cheung, Wen-Xiong Wang* Atmospheric, Marine, Coastal Environment Program, and Department of Biology, The Hong Kong University of Science and Technology (HKUST), Clear Water Bay, Kowloon, Hong Kong SAR *Corresponding author. Email: wwang@ust.hk ABSTRACT: Marine snails Thais clavigera accumulate high metal concentrations in their bodies and trophic transfer may play an important role in metal bioaccumulation in this top predator in the intertidal rocky shore. In this study, we examined the relationship between the subcellular metal distribution in prey (barnacles, mussels, oysters, herbivorous snails, limpets) and the assimilation efficiency (AE) of cadmium, silver and zinc in T. clavigera. The metal subcellular distributions in the oyster prey were also modified and the metal AEs in T. clavigera measured. We further purified the subcellular fractions of different prey and determined how the biochemical properties of different fractions affected the metal AEs. Results showed that the AEs of each metal from different prey were comparable and generally high (50 to 90%). Significant positive correlation was found between the Cd AEs and the metallothionein-like protein (MTLP) fraction, and between the AEs of Zn and the trophically available metal (TAM) fraction. For Ag, no relationship between its AE and any of the subcellular fractions was documented. When T. clavigera fed on oysters with different exposure regimes, the metal AEs were not significantly correlated with the metal subcellular partitioning in the oysters. Furthermore, the AEs of Ag, Cd and Zn were similar among the different biochemical fractions. For these 3 metals, T. clavigera assimilated 60 to 85% from the insoluble fraction, 40 to 80% from the heatsensitive protein fraction, 45 to 90% from the MTLP fraction, and 40 to 80% from the metal-rich granule (MRG) fraction. Our results imply that metals bound to the insoluble fraction or MRG were also bioavailable to T. clavigera. This study may help to better understand the mechanisms of metal transfer along the intertidal food chain. KEY WORDS: Whelks · Metals · Subcellular compartment · Trophic transfer · Assimilation Full text in pdf format PreviousNextExport citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 286. Online publication date: February 02, 2005 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2005 Inter-Research.

Internal metal sequestration and its ecotoxicological relevance: a review.

Organisms are able to control metal concentrations in certain tissues of their body to minimize damage of reactive forms of essential and nonessential metals and to control selective utilization of essential metals. These physiological aspects of organisms are not accounted for when assessing the risk of metals in the environment. The Critical Body Residue (CBR) approach relates toxicity to bioaccumulation and biomagnification and might at first sight provide a more accurate estimation of effects than the external concentration. When expressing CBRs on total internal concentrations, the capacity of organisms to sequester metals in forms that are not biologically reactive is neglected. The predictability of toxic effects will increase when knowledge on metal compartmentalization within the organisms' body is taken into account. Insight in metal compartmentalization sheds light on the different accumulation strategies organisms can follow upon metal exposure. Using a fractionation procedure to isolate metal-rich granules and tissue fragments from intracellular and cytosolic fractions, the internal compartmentalization of metals can be approximated. In this paper, current knowledge regarding metal compartmentalization in organisms is summarized, and metal fractions are identified that are indicators of toxicity. Guidance is provided on future improvement of models, such as the Biotic Ligand Model (BLM), for risk assessment of metal stress to biota.

SRXRF microprobe as a technique for studying elements distribution in Elsholtzia splendens

Elsholtzia splendens is a copper tolerant plant growing in copper mine areas in south of China and accumulates considerable heavy metals in plant tissue. In this study, synchrotron radiation X-ray fluorescence spectroscopy (SRXRF) microprobe was used to study the Cu and other elements distribution in E. splendens. The element (P, S, Cl, K, Ca, Mn, Fe, Cu, Zn) in the leaf epidermis and cross-sections of the stem and leaf could be checked by SRXRF which was considered a sensitive technique for trace element analysis. The highest Cu levels were measured in the vascular tissues of stem and petiole, while Cu levels in mesophyll were higher than in leaf epidermis. The levels of most elements were not higher in trichomes than in other tissues. It seems that the celluar compartmentation of heavy metals in epidermis and epidermal trichomes was not the general feature of all plants. There was a significant correlation between Cu and P, S, Ca in distribution, which suggested P, S, and Ca played an important role in Cu accumulation of E. splendens. Based on the significant correlation between Cu and elements Mn, Fe, and Zn in distribution, it seemed that Cu, Mn, Fe, and Zn could be transported by the same transporters with a broad substrate range.

Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by x-ray absorption spectroscopy.

Extended x-ray absorption fine structure measurements were performed on frozen hydrated samples of the cadmium (Cd)/zinc (Zn) hyperaccumulator Thlaspi caerulescens (Ganges ecotype) after 6 months of Zn(2+) treatment with and without addition of Cd(2+). Ligands depended on the metal and the function and age of the plant tissue. In mature and senescent leaves, oxygen ligands dominated. This result combined with earlier knowledge about metal compartmentation indicates that the plants prefer to detoxify hyperaccumulated metals by pumping them into vacuoles rather than to synthesize metal specific ligands. In young and mature tissues (leaves, petioles, and stems), a higher percentage of Cd was bound by sulfur (S) ligands (e.g. phytochelatins) than in senescent tissues. This may indicate that young tissues require strong ligands for metal detoxification in addition to the detoxification by sequestration in the epidermal vacuoles. Alternatively, it may reflect the known smaller proportion of epidermal metal sequestration in younger tissues, combined with a constant and high proportion of S ligands in the mesophyll. In stems, a higher proportion of Cd was coordinated by S ligands and of Zn by histidine, compared with leaves of the same age. This may suggest that metals are transported as stable complexes or that the vacuolar oxygen coordination of the metals is, like in leaves, mainly found in the epidermis. The epidermis constitutes a larger percentage of the total volume in leaves than in stems and petioles. Zn-S interaction was never observed, confirming earlier results that S ligands are not involved in Zn resistance of hyperaccumulator plants.

Compartmentalization of metals within the diverse colloidal matrices comprising activated sludge microbial flocs.

Activated sludge floc from a wastewater treatment system was characterized, with regard to principal structural, chemical, and microbiological components and properties, in relation to contaminant-colloid associations and settling. Multiscale analytical microscopies, in conjunction with multimethod sample preparations, were used correlatively to characterize diverse colloidal matrices within microbial floc. Transmission electron microscopy, in conjunction with energy dispersive spectroscopy (EDS), revealed specific associations of contaminant heavy metals with individual bacterial cells and with extracellular polymeric substances (EPS). Floc structure was mapped from the level of gross morphology down to the nano-scale, and flocs were described with respect to settling properties, size, shape, density, porosity, bound water content, and EPS chemical composition; gross surface properties were also measured for correlation with principal floc features. Compartmentalization results based on 171 EDS analyses and representative high-resolution images showed that nano-scale agglomerations of (i) silver (100%) and (ii) zinc (91%) were confined almost entirely to EPS matrices while (iii) Pb (100%) was confined to intracellular granules and (iv) aluminum was partitioned between EPS matrices (41%) and intracellular matrices (59%). The results suggest that engineered changes in microbial physiology and/or in macromolecular EPS composition may influence metal removal efficiencies.

Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM)

Many aspects of metal accumulation in aquatic invertebrates (i.e. toxicity, tolerance and trophic transfer) can be understood by examining the subcellular partitioning of accumulated metal. In this paper, we use a compartmentalization approach to interpret the significance of metal, species and size dependence in the subcellular partitioning of Cd and Zn in the bivalves Macoma balthica and Potamocorbula amurensis. Of special interest is the compartmentalization of metal as metal- sensitive fractions (MSF) (i.e. organelles and heat-sensitive proteins, termed 'enzymes' hereafter) and biologically detoxified metal (BDM) (i.e. metallothioneins (MT) and metal-rich granules (MRG)). Clams from San Francisco Bay, CA, were exposed for 14 d to seawater (20 ‰ salinity) containing 3.5 µg l -1 Cd and 20.5 µg l -1 Zn, including 109 Cd and 65 Zn as radiotracers. Uptake was followed by 21 d of depuration. The subcellular partitioning of metal within clams was examined following exposure and loss. P. amurensis accumulated ~22 × more Cd and ~2 × more Zn than M. balthica. MT played an important role in the storage of Cd in P. amurensis, while organelles were the major site of Zn accu- mulation. In M. balthica, Cd and Zn partitioned similarly, although the pathway of detoxification was metal-specific (MRG for Cd; MRG and MT for Zn). Upon loss, M. balthica depurated ~40% of Cd with Zn being retained; P. amurensis retained Cd and depurated Zn (~40%). During efflux, Cd and Zn concentrations in the MSF compartment of both clams declined with metal either being lost from the animal or being transferred to the BDM compartment. Subcellular compartmentalization was also size-dependent, with the importance of BDM increasing with clam size; MSF decreased accordingly. We hypothesized that progressive retention of metal as BDM (i.e. MRG) with age may lead to size dependency of metal concentrations often observed in some populations of M. balthica.

Cellular mechanisms for heavy metal detoxification and tolerance

Heavy metals such as Cu and Zn are essential for normal plant growth, although elevated concentrations of both essential and non-essential metals can result in growth inhibition and toxicity symptoms. Plants possess a range of potential cellular mechanisms that may be involved in the detoxification of heavy metals and thus tolerance to metal stress. These include roles for the following: for mycorrhiza and for binding to cell wall and extracellular exudates; for reduced uptake or efflux pumping of metals at the plasma membrane; for chelation of metals in the cytosol by peptides such as phytochelatins; for the repair of stress-damaged proteins; and for the compartmentation of metals in the vacuole by tonoplast-located transporters. This review provides a broad overview of the evidence for an involvement of each mechanism in heavy metal detoxification and tolerance.

Cellular mechanisms for heavy metal detoxification and tolerance

Heavy metals such as Cu and Zn are essential for normal plant growth, although elevated concentrations of both essential and non‐essential metals can result in growth inhibition and toxicity symptoms. Plants possess a range of potential cellular mechanisms that may be involved in the detoxification of heavy metals and thus tolerance to metal stress. These include roles for the following: for mycorrhiza and for binding to cell wall and extracellular exudates; for reduced uptake or efflux pumping of metals at the plasma membrane; for chelation of metals in the cytosol by peptides such as phytochelatins; for the repair of stress‐damaged proteins; and for the compartmentation of metals in the vacuole by tonoplast‐located transporters. This review provides a broad overview of the evidence for an involvement of each mechanism in heavy metal detoxification and tolerance.

Cellular and molecular aspects of metal sequestration and toxicity in earthworms

Summary Metals accumulated within the tissues of earthworms are not homogeneously distributed. Rather, they are sequestered predominantly within the posterior alimentary fraction. The clear organotropism of non-essential metals is reinforced by the subcellular compartmentation of metals according to their known ligand-binding affinities: in earthworm chloragocytes and intestinal epithelial cells, in situ X-ray mapping in high-pressure frozen thin cryosections revealed that Pb, Zn, Ca and P were co-distributed in a discrete subcellular compartment, whilst Cd and S were co-distributed in another. Tissue homogenization and fractionation confirmed these differences. Cd is sequestered by cysteine-rich metallothionein isoforms; one isoform may be a true Cd-detoxification protein because it bears two putative glycosylation sites, and may thus deliver Cd to the lysosomal system for cytological isolation. Metal accumulation imposes metabolic costs that can reduce somatic growth and/or reproduction in earthworms: the sequestered bioinactive metal fraction “diverts” energy into enhanced metallothionein synthesis and associated processes; the bioavailable metal fraction(s) may cause direct toxicological damage by competitive inhibition of metalloenzymes and metal-dependent transcription factors, and indirect damage if repair and compensatory stress responses are invoked. Molecular responses to metal-exposure stress are, in principle, linked to whole organism life-cycle parameters which, in turn, are ecologically relevant.

The distribution and intracellular compartmentation of metals in the endogeic earthworm Aporrectodea caliginosa sampled from an unpolluted and a metal-contaminated site

The tissue distribution of Cd, Cu, Pb, Zn and Ca in the endogeic earthworm Aporrectodea caliginosa living in a non-polluted and a heavy metal polluted soil was investigated. The tissues of animals from the contaminated soil contained greater concentrations of Cd, Pb and Zn than the corresponding tissues of animals from the unpolluted soil. The greatest concentrations of Cd, Pb, Zn, and Ca were primarily accumulated within the posterior alimentary canal (PAC), a tissue fraction which contained the greatest proportion of the whole-worm burdens of the respective metals. Cu was distributed fairly evenly in the tissue fractions investigated. The pattern of accumulation for the ‘heavy’ metals is broadly similar to that for epigeic earthworms; in contrast, a different pattern of tissue accumulation was found for Ca. In animals from the uncontaminated site, the major elemental constituents of the chloragosomes were P, Ca, Zn and S. A significant positive correlation exists between P and Ca within the chloragosomal matrix. These intracellular vesicles are major foci for Pb and Zn accumulation within the PAC, with ‘excess’ metals associated with P ligands within the chloragosome matrix. The incorporation of Pb and Zn appears to involve the cationic displacement of Ca. Such compartmentation appears to prevent dissemination of large concentrations of these metals into other earthworm tissues, and may thus represent a detoxification strategy based on accumulative immobilization. No intracellular localization of Cd was identified in the study, although the Cd concentration in the metalliferous soils examined was not exceptionally high. The observations are discussed in the context of a contribution to enhanced understanding of metal ecotoxicology in earthworms by providing baseline data on a little investigated ecophysiological group of earthworms. Comparisons of metal distribution and mechanisms of metal sequestration are made with other ecophysiological groups of earthworms, and the significance of the findings to biomonitoring and toxicity-testing programmes is considered.

Drift corrected quantitative elemental mapping in freeze-dried thin cryosections: Metal compartmentation within earthworm chloragocytes

Drift corrected quantitative elemental mapping in freeze-dried thin cryosections: Metal compartmentation within earthworm chloragocytes

Intracellular compartmentation of metals in aquatic organisms: roles in mechanisms of cell injury.

The intracellular compartmentation of essential and toxic metals is of intense scientific interest because of its potential for adding to our understanding of both normal homeostatic mechanisms for metals and of the mechanisms which underlie metal-induced cell injury. High-affinity metal-binding proteins, lysosomes, and precipitates such as inclusion bodies or concretions, play major roles in the regulation of divalent-metal cation bioavailability. The contribution of a given compartment toward metal homeostasis is dependent upon the level exposure, cell type, organ, species, and life cycle of the organism. Toxic metals may move between these compartments, but the rates and determinants of such exchanges have not been characterized. Available data clearly indicate that sequestration of toxic metals in these specialized compartments can produce profound disturbances in the subcellular handling of essential metals. Further studies of the mechanisms by which metals partition and/or transfer among these compartments are essential to understand and predict toxicity of this important class of toxic agents.

Intracellular Compartmentation of Metals in Aquatic Organisms: Roles in Mechanisms of Cell Injury

The intracellular compartmentation of essential and toxic metals is of intense scientific interest because of its potential for adding to our understanding of both normal homeostatic mechanisms for metals and of the mechanisms which underlie metal-induced cell injury. High-affinity metal-binding proteins, lysosomes, and precipitates such as inclusion bodies or concretions, play major roles in the regulation of divalent-metal cation bioavailability. The contribution of a given compartment toward metal homeostasis is dependent upon the level exposure, cell type, organ, species, and life cycle of the organism. Toxic metals may move between these compartments, but the rates and determinants of such exchanges have not been characterized. Available data clearly indicate that sequestration of toxic metals in these specialized compartments can produce profound disturbances in the subcellular handling of essential metals. Further studies of the mechanisms by which metals partition and/or transfer among these compartments are essential to understand and predict toxicity of this important class of toxic agents.

Preface

ArticlesOpen AccessPreface Bruce A. Fowler Bruce A. Fowler Search for more papers by this author Published:1 March 1986https://doi.org/10.1289/ehp.65-1474702Cited by:1AboutSectionsPDF ToolsDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InReddit "Preface." Environmental Health Perspectives, 65, p. 3FiguresReferencesRelatedDetailsCited byFowler B (2018) Intracellular compartmentation of metals in aquatic organisms: roles in mechanisms of cell injury., Environmental Health Perspectives, 71, (121-128), Online publication date: 1-Apr-1987. Vol. 65March 1986Metrics About Article Metrics Publication History Originally published1 March 1986Published in print1 March 1986 Financial disclosuresPDF download License information EHP is an open-access journal published with support from the National Institute of Environmental Health Sciences, National Institutes of Health. All content is public domain unless otherwise noted. Note to readers with disabilities EHP strives to ensure that all journal content is accessible to all readers. However, some figures and Supplemental Material published in EHP articles may not conform to 508 standards due to the complexity of the information being presented. If you need assistance accessing journal content, please contact [email protected]. Our staff will work with you to assess and meet your accessibility needs within 3 working days.