Effect of heavy metals on substrate utilization pattern, biomass, and activity of microbial communities in a reclaimed mining wasteland of red soil area

Abstract

The microbial biomass, basal respiration, and substrate utilization pattern in a copper mining wasteland of red soil area, southern China, were investigated, and indicated that soil microflora were obviously affected by heavy metals. Microbial biomass and basal respiration were negatively affected by comparatively high heavy metal levels. Two important microbial ecophysiological parameters, namely, the microbial biomass C (C_mic)/microbial biomass N (N_mic) ratio and the metabolic quotient (qCO₂) were significantly correlated to heavy metal stress. There was a significant decrease in the C_mic/N_mic ratio and an increase in the metabolic quotient with increasing metal concentration. Multivariate analysis of Biolog data for sole carbon source utilization pattern demonstrated that heavy metal pollution had a significant impact on microbial community structure and functional diversity. All the results showed that soil microbiological parameters could have great potential as sensitive, effective, and liable indicators of the stresses or perturbations in soils of mining ecosystems.

Introduction

Heavy metals are inherent components of soils, but a great concern today is related to their accumulation due to anthropogenic activities. Heavy metal pollution cannot only result in adverse effects on various parameters relating to plant quality and yield but also cause changes in the size, composition, and activity of the microbial community (Giller et al., 1998). Abiotic stress caused by heavy metals, in inorganic and organic forms, affects the growth, morphology, and metabolism of the microorganisms in soils. Numerous studies have demonstrated the adverse effect of different heavy metals on soil microbial biomass and activity (Doelman, 1985; Duxbury, 1985).

With the decline of many ecosystems in the world and the lack of knowledge of soil microbial communities, increasing awareness concerning the importance of soil microorganisms in terrestrial ecosystems has emerged (Yao et al., 2003). Soil microorganisms constitute a large dynamic source and sink of nutrients in all ecosystems and play a major role in plant litter decomposition and nutrient cycling, soil structure, nitrogen fixation, mycorhizal associations, reduction in plant pathogens, and other alternations in soil properties influencing plant growth (Kennedy and Smith, 1995). Moreover, they are very sensitive to environmental change and not only directly influence soil fertility levels (Insam et al., 1996) but also influence the microbial viability, microbial biomass turnover, and microbial utilization efficiency of organic carbon, which are important indicators of soil environmental quality (Bardgett et al., 1994).

A number of soil microbiological parameters, notably microbial biomass, basal respiration, and microbial community structure (Doran and Parkin, 1994; Sparling, 1997), have been suggested as possible indicators of soil environmental quality, and have been employed in national and international monitoring programs (Yao et al., 2000). Soil microbial biomass, which plays an important role in nutrient cycling and ecosystem sustainability, has been found to be sensitive to increased heavy metal concentrations in soils (Giller et al., 1998; Huang and Khan, 1998). Carbon dioxide evolution, the major product of aerobic catabolic processes in the carbon cycle, is also commonly measured and indicates the total carbon turnover. The metabolic quotient, i.e., the ratio of basal respiration to microbial biomass, is inversely related to the efficiency with which the microbial biomass uses the indigenous substrates (Anderson and Domsch, 1990) and can be a sensitive indicator for revealing heavy metal toxicity under natural conditions (Wardle and Ghani, 1995). More recently, microbial community structure has also been recommended as a biological indicator of heavy metal stress (Doelman et al., 1994). The assay is based on the Biolog system using 95 different carbon sources to produce a metabolic profile of microorganisms (Garland and Mills, 1991). It has been used to detect differences between microbial communities in soil and the rhizosphere, heavy metal polluted and unpolluted soil (Knight et al., 1997; Baath et al., 1998).

Recently, more and more attention has been paid to heavy metal contamination in tailings and there is a growing need to reclaim such sites to increase environmental quality after mining operations have ended. Ecological restoration and mine reclamation have become important parts of the sustainable development strategy of many countries. But most studies focused on the process of vegetation restoration and engineering technology of mine soil ecological systems, rather than underground soil microbe rehabilitation, evolvement, and effect on the ecological system of the mine area (Tordoff et al., 2000). However, an increasing body of evidence suggests that microorganisms are far more sensitive to heavy metal stress than soil animals or plants growing on the same soils (Giller et al., 1998). Thus, measures of the fate of the microbial community following the initiation of reclamation efforts or microbial responding would therefore serve as an indicator of the restoration progress (Harris et al., 1991) and may give insight into potential ways to accelerate restoration.

With increasing emphasis on fertility sustainability and environmental friendliness, restoration of soil microbial ecology has become important since the negative effects of heavy metals on plant growth and their possible entry into the food chain have been well documented (Yao et al., 2003). In this study, we measured a range of microbiological parameters in a reclaimed mining wasteland of red soil area, southern China. The aim of this study was to investigate the negative effect of heavy metal contamination on soil microorganisms and to assist in providing theoretical arguments on the quality evaluation and bioremediation of polluted soil in the mining area.