Elsevier

Environmental Pollution

Volume 110, Issue 1, October 2000, Pages 115-125
Environmental Pollution

Effect of soil on microbial responses to metal contamination

https://doi.org/10.1016/S0269-7491(99)00288-2Get rights and content

Abstract

An experiment was conducted to investigate microbial responses to metal inputs in five soils with varying clay and organic contents; one soil had also a higher pH. These soils were treated with a low metal, sewage sludge control or with this sludge contaminated to achieve Cu=112, Ni=58 and Zn=220 mg kg−1 in medium and Cu=182, Ni=98 and Zn=325 mg kg−1 in high metal soils. CO2 evolution rates were measured at 1 week and at 4–5-day intervals thereafter until the end of the incubation (7 weeks). Extractable metals (CaCl2 and water), biomass C, metabolic quotient, ergosterol, bacterial–fungal phospholipid fatty acid (PLFA — 3 weeks only) ratio and mineral N were measured at 3 and 7 weeks. Metal inputs caused a marked increase in metal availability in the slightly acidic sandy loams, a smaller increase in slightly acidic clays and had little effect in the alkaline loam. After an initial increase in CO2 evolution with metal inputs in all soils, the high metal treatment alone caused a significant decrease at later stages, mainly in sandy loams. Although biomass C and metabolic quotient decreased in all soils with higher metal inputs, the effect was more pronounced in the sandy loams. Metal inputs increased ergosterol and decreased bacterial–fungal PLFA ratios in most soils. Larger mineral N contents were found in all high metal soils at 3 weeks but, after 7 weeks, metals caused a significant decrease in sandy loams. CaCl2 and water-extractable Cu, Ni and Zn contents were closely correlated with microbial indices in sandy loam but not in clay soils. Overall, the effect of treatments on microbial and extractable metal indices was greater in loams. Within a single series, higher organic soils showed less pronounced responses to metal inputs, although this trend was not always consistent.

Introduction

Although metals such as Cu, Ni and Zn are essential nutrients for living organisms (Alloway, 1995), they may be toxic at high concentrations. Soil metal content is determined by the nature of the parent material and by inputs of metals from sources such as sewage sludge, mining and smelting, impurities in agricultural and horticultural materials and fossil fuel combustion. Atmospheric deposition results in diffuse contamination, whereas a more concentrated contamination arises where sewage sludge, metal-containing pesticides or fertilisers are used extensively (McGrath et al., 1995). Owing to its relatively high concentrations of metals, sewage sludge is a major potential source of metals in agricultural soils to which it is applied to improve fertility (Smith et al., 1989) and physical conditions (Pagliai et al., 1981).

Soil microorganisms play an essential role in the decomposition of soil organic matter. Any reduction in the diversity or abundance of microorganisms may affect the cycling of plant nutrients in the soil (Giller et al., 1998). Any disturbance to the soil ecosystem can disrupt microbial activity and hence nutrient cycling.

Numerous laboratory and field studies have demonstrated the adverse effect of metals on the soil ecosystem. Significant reductions in microbial biomass have been found in metal-contaminated compared to uncontaminated soil Frostegård, 1993b, Fließbach et al., 1994, Leita et al., 1995. Soil respiration responses to metal contamination are, however, less consistent. Doelman and Haanstra, 1984, Bååth et al., 1991, Hattori, 1992 found a significant decrease in CO2 evolution in metal-contaminated soil. In contrast, others Bardgett and Saggar, 1994, Fließbach et al., 1994 reported increased CO2 evolution in metal-polluted soils. These differing findings may result from variations in levels of metal contamination, in the source of the contamination (e.g. sewage sludge or mining), in the period of time over which responses were monitored and in characteristics of the receiving soil. Mineral N responses to metal contamination, which are usually positive, have been attributed to higher mineralization rates and the release of N from dead microbial cells (Bogomolov et al., 1996), and to decreased microbial immobilisation (Westermann and Tucker, 1974).

Studies have shown that metal contamination causes also a shift within the soil microbial community from sensitive to less sensitive microorganisms Maliszewska et al., 1985, Giller et al., 1989. Some species may be eliminated whilst others increase in abundance because of reduced competition for substrate (van Beelen and Doelman, 1997). The replacement of sensitive by resistant species may not result in any net effect on broad microbial indices such as soil respiration or total biomass.

As noted above, contradictory findings in relation to microbial responses to soil contamination may be due, at least in part, to variations in metal availability between different soils. Changes in organic matter and clay content can markedly affect the microbial availability of metals in soils (Dar, 1996).

Only limited research has been carried out into the influence of soil type on microbial responses to metal inputs (e.g. Hattori, 1991). Most comparisons between soils are reported in reviews of studies where experimental procedures are not always comparable (e.g. Giller et al., 1998). Also, the natural variability of soils, and the effects of management on organic matter contents and pH, make it difficult to specify a particular index which represents the effect of increased metal concentrations on soil microorganisms (Huysman et al., 1994). The aim of the study reported here was to investigate the combined effect of metals (Cu, Ni, Zn), applied at rates close to current UK limits (DoE, 1989), on a wide range of microbial indices in five soils with contrasting properties. The main hypothesis was that soils differing in their clay and organic contents would have varying metal availability and that these variations would influence any toxic effects on microorganisms. Metals were added in sewage sludge since this is a major pathway for metal input to agricultural soils and there is evidence (Aoyama et al., 1993) that metals are less toxic when applied with organic wastes than where they are applied as mineral salts.

Section snippets

Materials and methods

The experiment involved incubating five different soils, amended with three sludges of varying metal content, in flasks under controlled conditions (in the dark at 20±1°C). Respiration measurements started after 1 week and were repeated at 4–5-day intervals to the end of the experiment at 7 weeks. Extractable metals, pH, microbial indices, and mineral N in soils were measured after 3 weeks, in the final stages of a period of marked decline in microbial respiration, and at the end of the

Soil analyses

Soil pH and extractable metal data are presented in Table 3, Table 4 . The pH of all soils at 3 and 7 weeks was lower than that prior to treatment, with this reduction being more pronounced in the Rufford (RA, RG) soils. Increased metal inputs caused a progressive decline in pH, although these effects were small in comparison to soil differences. Water-extractable Cu and Zn concentrations decreased between weeks 3 and 7, whereas Ni concentrations increased. Over the same period, CaCl2

Discussion

The main hypothesis in the present study was that metal availability is controlled by soil physicochemical properties and that, for this reason, similar inputs of metals to contrasting soils may have differing effects on biological activity. The discussion will concentrate on this aspect of the experimental findings.

In a previous study, Hattori (1992) found that metals inhibited CO2 evolution more in a soil with low organic matter and cation exchange capacity (4.4 meq 100 g−1) than in a soil of

Conclusions

It can be concluded that variations in soil properties have a major effect on the proportion of the total metals present in sludge to which microorganisms are exposed and that these variations affect microbial response, at least in the short term. Metal inputs in sludges within current UK limits affected microbial populations and their activity, findings consistent with those of Fließbach et al. (1994). Although soil pH influences the availability of metals and their toxicity, the role of

Acknowledgements

The first author acknowledges the Ministry of Education, Government of Pakistan for financial support for this project. Thanks are also due to Dr. Gwyn Griffith, Institute of Grassland and Environmental Research, Aberystwyth, UK, for his assistance in ergosterol and PLFA determinations.

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