Accumulation of metals by microorganisms — processes and importance for soil systems

Abstract

Metal accumulation by solid substances can counteract metal mobilization in the environment if the solid substance is immobile. Microorganisms have a high surface area-to-volume ratio because of their small size and therefore provide a large contact area that can interact with metals in the surrounding environment. Microbial metal accumulation has received much attention in the last years due to the potential use of microorganisms for cleaning metal-polluted water. However, considerably less attention has been paid to the role of microorganisms for metal mobility in soil even though the same processes may occur there. Therefore, this paper highlights this area. The different accumulation processes that microorganisms perform are analyzed and their potential significance in soil systems is discussed.

Different kinds of mechanisms can be involved in the accumulation of metals by microorganisms, e.g. adsorption, precipitation, complexation and active transport into the cell. Physicochemical parameters like pH and ionic composition, as well as biological factors are of importance for the magnitude of accumulation. Often large amounts of metals can be accumulated with varying specificity, and microorganisms may provide nucleation sites for mineral formation.

Several studies of microbial metal accumulation have been made with different methods and aims. Most of these studies concern single-component systems with one organism at a time. Data from accumulation experiments with pure cultures of microorganisms have been used to model the overall metal retention in soil. A further development is experimental model systems using various solid soil components in salt medium.

Microbial metal accumulation is difficult to study in situ, but some experimental methods have been applied as tools for studying real soil systems, e.g. litter bags buried in soil containing microorganisms, a method where discs with microorganisms have been put onto agar plates with soil extracts, and comparison of sterilized and non-sterilized soils or soils with or without nutrient amendment.

Different aspects of microbial metal accumulation are emphasized with the different methods applied. Single-component systems have the advantage of providing excellent information of the metal binding properties of microorganisms but cannot directly be applied to metal behavior in the heterogenous systems that real soils constitute. Studies focused on the behavior of metals in real soils can, in contrast, provide information on the overall metal distribution but less insight into the processes involved. Obviously, a combination of approaches is needed to describe metal distribution and mobility in polluted soil such as areas around mines. Different kinds of multi-component systems as well as modelling may bridge the gap between these two types of studies. Several experimental methods, complementary to each other and designed to allow for comparison, may emphasize different aspects of metal accumulation and should therefore be considered.

To summarize, there are studies that indicate that microorganisms may also accumulate metals in soil and that the amounts may be considerable. However, much work remains to be done, with the focus of microorganisms in soil. It is also important to put microbial metal accumulation in relation to other microbial processes in soil, which can influence metal mobility, to determine the overall influence of soil microorganisms on metal mobility, and to be able to quantify these processes.

Introduction

The use and dispersion of metals has increased vastly during the 20th century, and the behavior of metals in the environment is therefore a matter of rising concern. Metals, like all elements, are not biodegradable and can only be transformed from one chemical state to another. The progressing regional acidification accelerates the spreading of metals by changing them into free, hydrated metal ions and thereby rendering them more mobile. Therefore, there is a considerable need for improved knowledge of metal mobilizing and retarding processes.

Metal accumulation by solid substances can counteract metal mobilization in the environment if the solid substance is immobile. Microorganisms have a high surface area-to-volume ratio because of their small size and therefore provide a large contact area that can interact with metals in the surrounding environment. Microbial metal accumulation has received much attention during the last years due to the potential use of microorganisms for cleaning metal-polluted water. However, less attention has been paid to the role of microorganisms for metal mobility in soil even though the same processes might occur there.

This paper aims at highlighting microbial metal accumulation in soil. Firstly, a brief overview of several interactions between metals and microorganisms is made to give a relevant background. Secondly, the different accumulation processes are reviewed. Finally, their significance in soil systems is outlined. In some cases, examples from environments other than soil are given to emphasize important mechanisms.

Some metals are essential to microorganisms and therefore required, whereas others are toxic even in small quantities. The composition and activity of the microflora will thus fluctuate in response to metal availability. Life in a polluted environment challenges the microorganisms in many ways, which is reflected in the fact that there is a greater demand for energy by microorganisms in order to cope with the toxicity of pollutants (Leita et al., 1995). The ability to grow at high metal concentrations is found in many organisms and may be the result of intrinsic or induced mechanisms, as well as environmental factors that may reduce metal toxicity (Gadd, 1992b). Gadd (1992a) defined tolerance as the ability to cope with metal toxicity by means of intrinsic properties of the organism. Resistance, on the other hand, would be the ability to survive toxic metals by detoxification mechanisms produced in direct response to the metal. Various mechanisms can be developed in response to the toxic metals, e.g. keeping or sending the metals outside of the organism by alkylation or efflux pumps, or transforming the metal into an innocuous form by production of metal binding compounds (see e.g. Wood and Wang, 1985, for a review). In many environments, metal pollution is accompanied by other conditions that are adverse to many microorganisms, like low concentration of organic matter and nutrients, as well as extreme pH values.

There are several ways in which microorganisms can influence metals, as summarized in Fig. 1:

(1) Some metals can be transformed, either by redox processes (e.g. Fe and Mn) or by alkylation (e.g. Hg). The mobility and toxicity of the transformed metal form usually differ significantly from that of the original.

(2) Accumulation of metals can occur either by metabolism-independent (passive) sorption or by intracellular, metabolism-dependent (active) uptake. Both processes may occur in the same organism. Intracellular, passive accumulation has been indicated in some cases. In the following, the terms sorption and adsorption are used when passive accumulation is considered, uptake is used when metabolism-dependent intracellular transport is implied and accumulation when a general term is needed. If a metal is accumulated by microorganisms, the fate of the metal will be closely tied to the fate of the microbial cells. On the one hand, microorganisms can be transported and any metal accumulated by them will therefore be mobile. On the other hand, in many systems, a large fraction of the microorganisms is immobile, and the metal can consequently be retained.

(3) Microorganisms can produce or release substances, for instance organic compounds that change the mobility of the metals, or sulfide that reduces the mobility of many metals.

(4) Microorganisms participate in the cycling of carbon and thereby influence the amount and character of organic matter. This can be of substantial importance for metal mobility, because organic compounds may bind metals. Microbial degradation of the metal–organic complex can change the speciation of the metal. However, metal binding to various organic substances may decrease the microbial degradation of the organic compound (see, e.g. Brynhildsen, 1992, Krantz-Rülcker et al., 1995). The result may be that non-degraded organic matter with metals associated accumulates.

(5) In addition to these direct processes, microorganisms can influence metal mobility indirectly since they affect pH, Eh, etc. All these processes should be kept in mind while studying the influence of microbial metal accumulation on metal mobility.