Shortened lifespan of nematode Caenorhabditis elegans after prolonged exposure to heavy metals and detergents

Abstract

The acute toxicities of heavy metals and detergents have been well examined with respect to several endpoints, such as mortality, for application to toxicity tests for environmental assessments. However, chronic influences of these agents on multicellular organisms still need to be determined. Here we studied long-term effects on the lifespan of a free-living nematode, Caenorhabditis elegans, resulting from prolonged exposure to heavy metals or detergents, as well as short-term inhibitory effects on reproduction and growth. These agents inhibited growth of hatched larvae and reproductive capacity in a concentration-dependent manner. They also effectively shortened the lifespan of the adult nematode over the same concentration range. Since toxic effects on both growth and lifespan were observed over similar concentration ranges, where acute toxicities in various endpoints are detected, the shortening of the lifespan can be used as a new endpoint for the assessment of various ecotoxic agents.

Introduction

Surfactants and heavy metals such as cadmium and copper have been present in industrial and household waste for many years, and extensive water and soil pollution has resulted, causing serious problems in developing countries. A noxious nonessential metal, cadmium is carcinogenic (Jin et al., 2003) and its bioaccumulation makes it potentially lethal (Kobayashi et al., 2002). Although copper is an essential metal for cellular functions, excess oral intake of copper can cause human lethality (Stewart and Lassiter, 2001). Some kinds of surfactants and detergents are also known to be hazardous to aquatic organisms (Lewis, 1990). Thus, it is important to study the toxic effects of these agents and to monitor their risk for humans and the environment.

A free-living nematode, Caenorhabditis elegans (C. elegans), is an abundant organism in soil ecosystems and plays key roles in decomposition and nutrient cycling (Sohlenius, 1980). It is also an excellent model organism because of its short lifespan (approximately 3 weeks at 20 °C under optimal conditions) and ease of manipulation. In addition, it is a simple multicellular eukaryote whose developmental process and behavior can easily be monitored under the microscope. By virtue of these properties, several toxicity tests using nematodes have been developed for ecological risk assessment in soil (Freeman et al., 1999; Peredney and Williams, 2000) and water (Freeman et al., 1998; Hitchcock et al., 1997; Traunspurger et al., 1997; Ura et al., 2002; van Kessel et al., 1989). These tests were shown to be effective in the detection of heavy metal contamination, including contamination by cadmium and copper, by monitoring the toxic effects on mortality (Freeman et al., 1998, Freeman et al., 1999; Hitchcock et al., 1997; Peredney and Williams, 2000; Ura et al., 2002), reproduction (Anderson et al., 2001; Dhawan et al., 1999), behavior (Anderson, 2001, Anderson, 2004; Boyd et al., 2003; Dhawan et al., 1999) and feeding (Anderson, 2001, Anderson, 2004; Boyd et al., 2003) as ecologically relevant endpoints. Additional endpoints reported for toxicity studies with this nematode include alteration of ultrastructures (Popham and Webster, 1979), stress protein induction (Guven et al., 1995; Wah Chu and Chow, 2002) and body length (Anderson et al., 2001; Popham and Webster, 1979; Traunspurger et al., 1997; van Kessel et al., 1989). Thus, several endpoints have been used for acute toxicity testing with C. elegans and the effects are assessed in relatively short-term treatments (2–72 h). Although it is likely that living organisms in polluted environments are continuously exposed to toxicants, for example by intake of foods and fluids, and are chronically damaged, few reports have examined long-term toxic effects, such as influences on the lifespans of the organisms in ecosystems. Thus, in this study, we have examined the long-term influence on the lifespan of the nematode C. elegans resulting from prolonged exposure to heavy metals (copper and cadmium) and detergents (sodium dodecyl sulfate and a commercially available surfactant), in addition to performing an assessment of the short-term effects on both reproduction and growth.