Elsevier

Aquatic Toxicology

Volume 93, Issue 1, 4 June 2009, Pages 53-60
Aquatic Toxicology

Differences in metal sequestration between zebra mussels from clean and polluted field locations

https://doi.org/10.1016/j.aquatox.2009.03.006Get rights and content

Abstract

Organisms are able to detoxify accumulated metals by, e.g. binding them to metallothionein (MT) and/or sequestering them in metal-rich granules (MRG). The different factors involved in determining the capacity or efficiency with which metals are detoxified are not yet known.

In this work we studied how the sub-cellular distribution pattern of cadmium, copper and zinc in whole tissue of zebra mussels from clean and polluted surface waters is influenced by the total accumulated metal concentration and by its physiological condition. Additionally we measured the metallothionein concentration in the mussel tissue. Metal concentration increased gradually in the metal-sensitive and detoxified sub-cellular fractions with increasing whole tissue concentrations. However, metal concentrations in the sensitive fractions did not increase to the same extent as metal concentrations in whole tissues. In more polluted mussels the contribution of MRG and MT became more important. Nevertheless, metal detoxification was not sufficient to prevent metal binding to heat-sensitive low molecular weight proteins (HDP fraction). Finally we found an indication that metal detoxification was influenced by the condition of the zebra mussels. MT content could be explained for up to 83% by variations in Zn concentration and physiological condition of the mussels.

Introduction

Accumulated metals in aquatic organisms can provide valuable information on metal bioavailability in the aquatic environment (Rainbow, 2002, Bervoets et al., 2005). However, total concentrations of accumulated metals in the tissues do not always give a reliable indication of metal toxicity (Cain et al., 2004, Vijver et al., 2004). Only that fraction of the metals that inappropriately interacts with physiologically sensitive target molecules (like small peptides, enzymes, DNA and RNA) or organelles (mitochondria, nuclei, membranes) is potentially toxic (Wallace et al., 2003, Wang and Rainbow, 2006, Wang and Wang, 2008). To regulate the internal availability of essential metals for metabolic functions and to avoid inappropriate binding of essential and non-essential metals to important bio-molecules, various sub-cellular systems have evolved. With this, essential metals in excess of metabolic requirements and non-essential metals are detoxified and/or excreted (Rainbow, 2002, Campbell et al., 2005, Campbell et al., 2008). Excess of metals can be bound to the metal binding protein metallothionein (Vijver et al., 2004, Van Campenhout et al., 2008) and (subsequently) immobilized within granules (Marigómez et al., 2002). Metal-rich granules can be excreted via faeces or basal exocytosis towards haemocytes (Desouky, 2006). Nevertheless, for non-essential metals, often no or very slow elimination is observed (Roditi et al., 2000, do Amaral et al., 2005).

Techniques like differential centrifugation (Wallace et al., 2003), chromatographic separation (Van Campenhout et al., 2008), and microscopic analysis (Marigómez et al., 2002) give the opportunity to study the internal distribution of the metals. However, it is not yet fully understood whether and how factors such as total tissue concentration, uptake rate and physiological condition are involved in the capacity of metal detoxification.

Biological factors such as genetic background (Knapen et al., 2004), size (Wallace et al., 2003), physiological condition of the organism, or uptake route (Ng et al., 2007) might be involved in the metal detoxification capacity. Metal detoxification and the maintenance of detoxification mechanisms might be energetically expensive. Therefore, the organisms in good condition might be able to invest more energy in metal detoxification. The energy status of an organism can give a good indication of its condition and can be determined by measuring energy stores (i.e. carbohydrates, proteins and lipids). Also condition-indices such as the tissue condition index (TCI) (weight normalized for size) and water content can give a valuable indication of the condition for several organisms (Smolders et al., 2004, Voets et al., 2006).

Mussels have been used extensively for monitoring water pollution. In the freshwater environment, zebra mussels have shown to be valuable monitoring organism. They are widespread, sedentary, easy to collect and handle and good accumulators. Furthermore, they might represent a significant entrance of metals in the ecological food chain and accumulate toxicants according to bioavailable levels in the environment (Hendriks et al., 1998, Kraak et al., 1991, Bervoets et al., 2005).

In this work we studied how zebra mussels under polluted conditions deal with an excess of accumulated Cd, Cu and Zn. To this, we studied how zebra mussels distribute excess of these accumulated metals sub-cellular and how this is influenced by the total metal concentration in the mussels. We also investigated whether the physiological condition of the mussels affects this sub-cellular distribution and/or if there is a relation between the physiological condition and the concentration of metals in the so-called metal-sensitive fractions.

To achieve these goals, we determined the sub-cellular distribution of Cd, Cu and Zn in whole tissue of zebra mussels from clean and polluted surface waters in Flanders, Belgium. We measured the metallothionein concentration. We defined the condition of the mussels by measuring the tissue condition index (TCI).

Section snippets

Sampling sites

Mussels were sampled in September 2005 from two lakes (ponds) and two canals in Flanders (Belgium) with different levels of metal pollution. The selection of the locations was based on previous measurements of metal levels in zebra mussel tissue (Bervoets et al., 2005). Lake Walenhoek in Niel (further referred to as Loc1) was selected as a clean location. The lake Nekker in Mechelen (further referred to as Loc2) was slightly polluted, the Albert canal in Schoten (further referred to as Loc3)

Metal accumulation

Metal concentrations in whole tissue of zebra mussels ranged from 0.69 to 40.6 nmol/g (w/w) for Cd, from 16.9 to 79.0 nmol/g (w/w) for Cu and from 136.8 to 284.5 nmol/g (w/w) for Zn. Metal accumulation in zebra mussels (Cd, Cu and Zn) showed significant differences among the sampling sites (Fig. 2a–c). Cd, Cu and Zn levels in the mussels were highest in mussels from Loc4, followed by mussels from Loc3 and Loc2.

Sub-cellular metal compartmentalization

The distribution of the metals over the different sub-cellular fractions, determined by

Discussion

Metal levels in the mussels ranged from low to very high concentrations depending on the exposure location. The lowest metal levels, measured in mussels from Loc1, were comparable to levels measured in the Ysselmeer and Markermeer (NL) (Hendriks et al., 1998), which are considered as good reference locations. Mussels from Loc2 had slightly elevated Cd and Zn concentrations. Mussels from Loc3 had elevated Cd and Cu concentrations and mussels from Loc4 were highly contaminated with Cd, Cu and Zn

Acknowledgments

This project was supported by the University of Antwerp via a Nieuw Onderzoeks Initiatief project of the Bijzonder Onderzoeks Fonds (BOF44704/UA). Furthermore, we would like to thank Lien Van Gool for the English revision.

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