The dissolution of sulfide minerals such as pyrite [FeS2], arsenopyrite [FeAsS], chalcopyrite [CuFeS2], sphalerite [ZnS], and marcasite [FeS2] yields hot, sulfuric acid-rich solutions that contain high concentrations of toxic metals. In locations where access of oxidants to sulfide mineral surfaces is increased by mining, the resulting acid mine drainage [AMD] may contaminate surrounding ecosystems. Communities of autotrophic and heterotrophic archaea and bacteria catalyze iron and sulfur oxidation, thus may ultimately determine the rate of release of metals and sulfur to the environment. AMD communities contain fewer prokaryotic lineages than many other environments. However, it is notable that at least two archaeal and eight bacterial divisions have representatives able to thrive under the extreme conditions typical of AMD. AMD communities are characterized by a very limited number of distinct species, probably due to the small number of metabolically beneficial reactions available. The metabolisms that underpin these communities include organoheterotrophy and autotrophic iron and sulfur oxidation. Other metabolic activity is based on anaerobic sulfur oxidation and ferric iron reduction. Evidence for physiological synergy in iron, sulfur, and carbon flow in these communities is reviewed. The microbial and geochemical simplicity of these systems makes them ideal targets for quantitative, genomic-based analyses of microbial ecology and evolution and community function.
1 Introduction
Acidic, metal-rich fluids are formed by chemical weathering of metal sulfide-rich rocks. These acid rock drainage [ARD] solutions are hot because metal sulfide oxidation reactions are highly exothermic. The predominant metal sulfide mineral in most rocks is pyrite [FeS2]. Pyrite-rich deposits are often mined for metals such as Au, Ag, Cu, Zn, and Pb, which are typically present as impurities in pyrite or occur in sulfide minerals such as chalcopyrite [CuFeS2], sphalerite [ZnS], and galena [PbS]. Mining increases the surface area of sulfide ores exposed to air and water, thus, increases rates of acid generation. Regions where rocks have low buffering capacity generate highly acidic toxic solutions that are referred to as acid mine drainage [AMD].
Despite the extreme acidity, heat, and high concentrations of sulfate and toxic metals, a diverse range of microorganisms populate AMD environments. These organisms can form a chemoautotrophically-based biosphere in the subsurface, ultimately sustained by electron donors derived from sulfide minerals, CO2, O2, and N2 derived from air, and phosphate liberated by water–rock interaction. Microbial activity increases the rate of AMD formation and may be responsible for the bulk of AMD generated [1].
Microbe–mineral interactions are of importance because AMD is a very widespread environmental problem. The organisms can be used in ore processing and are a source of novel biomolecules [especially enzymes] for industrial processes.
DNA-based studies of organisms populating mining environments have provided insights into the diversity of acidophilic, metal-tolerant species. Here, we review the importance of archaeal and bacterial lineages, and integrate microbiological, geochemical, mineralogical, and molecular information necessary for quantitative descriptions of the ecology of AMD. Eukaryotes [protists, fungi, and yeasts] are abundant and important in some parts of acid systems. However, due to the paucity of data on eukaryotes in AMD, our review focuses primarily on the prokaryotic components of these communities. We show that the prokaryotic richness of acidophilic communities is low compared to other extremophile and non-extremophile assemblages, yet the species are broadly distributed across the tree of life. Because of their biological and geochemical simplicity, AMD environments have potential as model systems for analysis of biogeochemical interactions and feedbacks and microbial community structure and function.
2 Dissolution of sulfide minerals
Many factors impact AMD generation. In part, rates of dissolution reactions are determined by fluid chemistry and flow, mineral and rock type, and temperature. The rate of supply of oxidant to the mineral surface influences the rate at which pyrite dissolves. The typical oxidants are oxygen and ferric iron. The concentration of oxygen in groundwater is very small compared to the large requirement for O2 in the overall reaction:
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Thus, the predominant source of oxygen in rapidly oxidizing systems is air. In fact, to create typical AMD, each packet of solution must be re-oxygenated hundreds to thousands of times along its flow path [2].
Geochemical studies have established that oxygen is a less effective sulfide oxidant than ferric iron. Thus, the dominant pathway for pyrite dissolution involves oxidation of ferrous iron by oxygen:
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followed by reduction of ferric iron by sulfide:
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Note that the sum of reactions in and , required to describe the sustainable process, yields the reaction in . Ferrous iron oxidation by O2 at low pH is slow, thus the rate of the reaction in may limit the rate of AMD generation. However, iron-oxidizing prokaryotes catalyze ferrous iron oxidation, thus can determine the rate of pyrite dissolution [1,3]. The feedback between metabolic activity and mineral dissolution can drive the pH down to values