Arsenic-Transforming Microbes and Their Role in Biomining Processes
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Environ Sci Pollut Res (2013) 20:7728–7739 DOI 10.1007/s11356-012-1449-0 MINING AND THE ENVIRONMENT - UNDERSTANDING PROCESSES, ASSESSING IMPACTS AND DEVELOPING REMEDIATION Arsenic-transforming microbes and their role in biomining processes L. Drewniak & A. Sklodowska Received: 15 October 2012 /Accepted: 19 December 2012 /Published online: 9 January 2013 # The Author(s) 2013. This article is published with open access at Springerlink.com Abstract It is well known that microorganisms can dissolve Introduction different minerals and use them as sources of nutrients and energy. The majority of rock minerals are rich in vital An ongoing challenge for the mining industry is the elements (e.g., P, Fe, S, Mg and Mo), but some may also development and application of efficient, low-cost and contain toxic metals or metalloids, like arsenic. The toxicity environmentally friendly methods of metal recovery. of arsenic is disclosed after the dissolution of the mineral, Considerable effort is currently devoted to the improve- which raises two important questions: (1) why do micro- ment of existing technologies, particularly those intended organisms dissolve arsenic-bearing minerals and release this for (1) metal recovery from low-grade ores, which has metal into the environment in a toxic (also for themselves) not been economic for many years, and (2) mine and form, and (2) How do these microorganisms cope with this wastewater treatment. A well-recognized way of extract- toxic element? In this review, we summarize current knowl- ing metals from mineral resources not accessible by edge about arsenic-transforming microbes and their role in conventional mining is the use of methods based on biomining processes. Special consideration is given to stud- microbial activity. Microbes permit the recovery of met- ies that have increased our understanding of how microbial als from primary mineral deposits and from secondary activities are linked to the biogeochemistry of arsenic, by raw materials like mine tailings, which may contain only examining (1) where and in which forms arsenic occurs in trace amounts of the desired elements (especially pre- the mining environment, (2) microbial activity in the context cious metals). In addition, biomining techniques are gen- of arsenic mineral dissolution and the mechanisms of arse- erally less energy-intensive and less polluting than most nic resistance, (3) the minerals used and technologies ap- non-biological procedures. plied in the biomining of arsenic, and (4) how microbes can The most common biomining processes involve oxida- be used to clean up post-mining environments. tive dissolution of minerals, leading to the solubilization of some metal compounds, and other become more accessible Keywords Arsenic minerals . Microbial activity . Arsenite to chemical extraction but remain in an insoluble form oxidation . Arsenate reduction . Bioleaching . (Rawlings 2011). Microbiological oxidative dissolution of Bioremediation minerals is mainly produced by the oxidation of iron, sulfur, or both of these typically results in the release of accompa- nying elements (e.g., oxidation of FeAsS leads to the release of iron and arsenic). In addition to desired metals, the oxidation of sulfur and iron minerals may sometimes cause the release of environmentally hazardous elements. One example of such troublesome deposits are minerals contain- Responsible editor: Robert Duran : ing arsenic, a toxic metalloid whose extraction is of little L. Drewniak (*) A. Sklodowska commercial importance. Laboratory of Environmental Pollution Analysis, In this review, we examine the microbial dissolution of Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland arsenic-bearing minerals as a side effect of biomining pro- e-mail: [email protected] cesses, with special emphasis on (1) the primary and Environ Sci Pollut Res (2013) 20:7728–7739 7729 secondary arsenic minerals that are the most abundant and bioweathering processes. The structure of arsenic sulfide dominant in mining environments, particularly those play- minerals is stabilized by (1) covalent bonds between arsenic ing key roles in microbial life cycles, (2) the current state of and sulfur, (2) coordination bonds between iron and arsenic knowledge on microbial activity in the context of arsenic or sulfur (O’Day 2006), and (3) van der Waals forces be- mineral dissolution and mechanisms of arsenic resistance, tween molecular units (Mullen and Nowacki 1972). Other (3) the minerals used and technology applied in biomining transition metals, such as Co, Ni and Cu, also combine with of arsenic-bearing minerals, and (4) how microbes are used arsenic and sulfur to form a variety of minor sulfides and to clean up post-mining environments. sulfosalts, often with extensive solid solution (Table 1). Sulfide minerals are also associated with a number of arsen- ides, including arsenic structures with Fe, Co, Ni and Cu. Arsenic minerals in mining environments These minerals are typically rare and occur in hydrothermal and magmatic ore deposits. Similar to sulfides, the chemical Arsenic is widely distributed in the Earth's crust, occurring bonds in arsenides are covalent. It is noteworthy that these in trace amounts (average crustal abundance =1.5 mg/kg), minerals often form solid solutions with each other and with predominantly in minerals of igneous and sedimentary rocks sulfide minerals in structural arrangements of common sul- and soils (Plant et al. 2005). Some arsenic-bearing minerals, fides (e.g., pyrite, pyrrhotite, marcasite, galena). such as arsenides and sulfarsenides, are considered non- Weathering and hydrothermal alteration of these primary toxic because they are highly insoluble. Problems arise minerals is thought to produce secondary arsenic minerals: when these primary minerals break down and enter into the arsenic (III) oxides (arsenites) and arsenic (V) oxides solution or form more soluble species such as oxides (arsenates) (Table 2). Simple arsenic (III) oxides (arsenolite (Vaughan 2006). Arsenic can be mobilized by dissolution and claudetite) occur as products of arsenic sulfide weath- into water or emitted into the atmosphere through natural ering, but they are more commonly produced by the roasting processes as well as anthropogenic activity. Of the many of arsenic-bearing ore minerals or coal. Due to their similar causes of arsenic contamination microbial activity, mining size and charge, arsenic (V) minerals (arsenates) are usually and smelting operations seem to be the most significant. considered as a subclass of the phosphate minerals (O’Day A thorough understanding of arsenic geochemistry is 2006), and as a result of this similarity, arsenate minerals necessary to be able to predict the likely impact of and occur in a variety of arsenic-rich soils and oxidized environ- potential risks associated with the use of microbes in bio- ments. Secondary arsenic minerals occur as weathering mining processes. A key question is where and in which products of arsenic-containing sulfidic metal deposits, form does arsenic occur in the mining environment? Knowl- where the sulfidic minerals are often coated with layers of edge concerning the type of minerals as well as the physical oxidized and hydrated arsenate minerals. The most common and chemical conditions occurring in the mine environment secondary arsenic mineral is scorodite. Less common but is vital in order to study how microbial activities are linked more environmentally important arsenic minerals are found to the biogeochemistry of arsenic. in mine-waste heaps and other types of industrial deposit. Other recognized secondary arsenic minerals are arsenolite, claudetite, erythrite, kankite and mimetite (Table 2). An Arsenic-bearing minerals excellent review of these minerals and their origin was presented in a special edition of Elements in 2006 (vol. 2, More than 200 minerals that contain arsenic are found in no. 2). nature (Hoang et al. 2010). Arsenic occurs mainly as arsen- Secondary arsenic minerals exhibit a wide range of sol- ides, sulfides, oxides, arsenates and arsenites. Most of these ubility. For example, arsenolite and claudetite, and some minerals are found in close association with metals such as calcium arsenates (haidingerite, pharmacolite), are highly Fe, Cu, Co, Ni, Cd, Pb, Ag and Au. soluble in water, whereas some iron arsenates, such as The most abundant arsenic ore minerals are As sulfides, beudantite, pharmacosiderite and scorodite, are relatively including arsenopyrite (FeAsS), realgar (As4S4) and orpi- insoluble. Sparingly soluble minerals can effectively immo- ment (As2S3). These primary arsenic minerals are formed bilize arsenic in contaminated sites and their precipitation only under high temperature conditions in the Earth’s crust decreases the amount of arsenic in the water. On the other and occur in hydrothermal and magmatic ore deposits. In- hand, the re-dissolution of secondary arsenic minerals as a terestingly, orpiment- and realgar-like minerals can be result of various environmental factors (pH increase, tem- formed in sulfate-reducing environments, probably by pro- perature, supply of new chemical compounds with water) cesses requiring microbiological sulfur and arsenic reduc- and especially microbial activity, may greatly affect the tion (O’Day et al. 2004). An important feature of each level of contamination of ground and surface waters by mineral is its stability in the face of weathering and arsenic species (Drahota and Filippi 2009). 7730 Environ Sci