–Microbe Interactions and Implications for Environmental Mitigation

Hailiang Dong1,2

1811-5209/12/0008-0113$2.50 DOI: 10.2113/gselements.8.2.113

lay minerals are ubiquitous in soils, sediments, and sedimentary rocks, Some of these interactions generate and they play important roles in environmental processes. Microbes distinct mineral assemblages in the ancient rock record, producing Care also abundant in these geological media, and they interact with biosignatures. clays via a variety of mechanisms, such as reduction and oxidation of struc- Although clay mineralogy has tural and mineral dissolution and precipitation through the production been studied for more than half a of siderophores and organic acids. These interactions greatly accelerate clay century and various applications mineral reaction rates. While it is certain that microbes play important roles have been developed, the impor- tant role of microbes in clay in transformations, quantitative assessment of these roles is mineral transformations has been limited. This paper reviews some active areas of research on clay–microbe recognized for only about 20 years. interactions and provides perspectives for future work. In the last decade, interest in this fi eld has risen dramatically, as it KEYWORDS: clay minerals, microorganisms, oxidation, reduction, transformation has become clear that reduced clays can sequester toxic metals INTRODUCTION and radionuclides and that clays can degrade organic compounds (Stucki and Kostka 2006; Clay minerals are likely the minerals that we encounter Dong et al. 2009). In this article, I will start with a short most commonly in our daily lives. They form the soils in review of clay mineralogy and then follow with a compre- which plants grow, and they are the primary materials in hensive overview of clay mineral–microbe interactions. I a range of products and applications, including cat litter, will end with a consideration of the environmental impli- animal feed, pottery, china, oil absorbants, pharmaceuti- cations of clay mineral–microbe interactions and the cals, cosmetics, wastewater treatment, and even antibacte- outlook for future developments. rial agents. Clay minerals such as and smectite have long been used to treat ailments of the digestive tract in certain countries (Ferrell 2008). CLAY MINERALOGY Clays are built of tetrahedral and octahedral sheets, typi- The diversity of clay mineral applications can be attributed cally in a 1:1 or 2:1 ratio. A 1:1 clay structure consists of to the chemistry and structure of these minerals. Clay one tetrahedral sheet and one octahedral sheet, and minerals are hydrous aluminum layer silicates with struc- tures similar to those of micas. Unlike the micas, however, interlayers of clay minerals contain a low cationic charge to “glue” adjacent silicate sheets, and water molecules can enter or exit the interlayer regions easily. Thus, these mate- rials swell or shrink under wet or dry conditions. Clays are common products of the weathering and hydrothermal alteration of various rocks, but they can also precipitate directly from aqueous fl uids. Because of their low-temper- ature genesis, clay minerals are very common in soils, sedi- ments, and sedimentary rocks. Depending on their specifi c mode of formation, clay minerals can form extensive deposits of economic value (FIG. 1). Because clay minerals are common in low-temperature environments where microorganisms thrive, the interac- tions between clays and microbes are important to a number of surfi cial processes. Microorganisms can dissolve, precipitate, and transform clay minerals and thus change their physical and chemical properties. Some of these changes are benefi cial, whereas others are not desirable.

1 State Key Laboratory of Biogeology and Environmental Geology This vermiculite deposit in Weili, Xinjiang, China, FIGURE 1 China University of Geosciences, Beijing, 100083, China was formed from the weathering of phlogopite by meteoric water. PHOTO COURTESY OF TONGJIANG PENG, SOUTHWEST 2 Department of Geology and Environmental Earth Science UNIVERSITY OF SCIENCE AND TECHNOLOGY, CHINA Miami University, Oxford, OH 45056, USA E-mail: [email protected] or [email protected]

ELEMENTS, VOL. 8, PP. 113–118 113 APRIL 2012 examples include kaolinite and serpentine. A 2:1 clay struc- trapping of hydrocarbons (Pevear 1999). Thus, the S-I reac- ture consists of an octahedral sheet sandwiched between tion is often used as an index for the generation of petro- two tetrahedral sheets (FIG. 2), and examples include smec- leum and natural gas. In terrigenous sediments, the S-I tite, illite, and vermiculite. reaction typically takes place over the temperature range of about 90–120 oC (Moore and Reynolds 1997). To better Of special importance are two 2:1 clay mineral families: understand the kinetics and the controlling conditions for smectite and illite (FIG. 3). Smectite minerals are 2:1 layer this reaction, laboratory simulation experiments are typi- silicates with a total negative charge between 0.2 and 0.6 cally performed (Huang et al. 1993). These efforts reveal per half unit cell. The low charge accounts for the capacity that, in the absence of any microbial activity, conditions of smectites to swell. A member of the smectite family of 250–350 °C and 50–100 MPa are often needed to achieve called nontronite (iron-rich smectite) has the following realistic reaction rates (a few months) (Huang et al. 1993; ideal formula: Kim et al. 2004). However, in the presence of microbial 3+ 2+ activity, this reaction occurs via various mechanisms, at (K0.01 Na0.30 Ca0.15)(Al0.55 Fe 3.27 Fe 0.06Mg0.12) 3+ much lower temperatures and pressures over shorter time (Si7.57Al0.15Fe 0.28)O20(OH)4 . durations. The large cations (Na+, Ca2+, and K+) enter the interlayer space to balance the net negative charge created by the MICROBE–CLAY MINERAL INTERACTIONS substitution of trivalent Al and Fe for tetravalent Si in the tetrahedral site and divalent Mg for trivalent Fe in the Microbial Dissolution of Clay Minerals octahedral site. In soils and sediments, microorganisms play important Illite minerals have the same basic structure as smectite, roles in the dissolution of clay minerals, contributing to but with a higher net negative layer charge of 0.6 to 0.9 elemental cycling, soil fertility, and water quality. Microbes per half unit cell, a result of the greater degree of tetrahe- accelerate clay mineral dissolution either through redox dral and/or octahedral substitution. A typical illite from reactions of structural iron (see below) or through the Silver Hill, Montana, USA, has the following formula: release of metabolic by-products. In contrast to abiotic dissolution where pH is a primary driving force, biotic 3+ 2+ (Mg0.09Ca0.06K1.37)(Al2.69Fe 0.76Fe 0.06Mg0.43Ti0.06) dissolution requires many organic compounds to destabi- (Si6.77Al1.23)O20(OH)4 . lize the mineral structure. These compounds include sider- ophores (a group of element-scavenging compounds that Because of the higher charge of the interlayer cations, the contribute to the weathering of Fe oxides and silicate electrostatic attraction between the basal surface and the minerals), organic acids, iron chelators (small organic interlayer cations is stronger in illite than in smectite. molecules that bind to Fe and help its transport), and extra- Consequently, illite does not expand when hydrated. cellular polymeric substances (high-molecular-weight Smectite is stable at low temperature and pressure, which compounds composed of polysaccharides that are secreted are the typical conditions in soils and surfi cial sediments. by microorganisms into the environment). In microbially As soils and sediments are buried, smectite becomes mediated clay mineral dissolution, the mineral surface unstable and transforms into illite according to the reactivity seems to play a secondary role (Grybos et al. 2011). following reaction: Microbially mediated mineral dissolution is usually incon- smectite + Al3+ + K+ → illite + silica . gruent, meaning that certain elements are removed pref- erentially relative to others, producing nonstoichiometric Three important variables drive the smectite-to-illite (S-I) minerals. Silica is a common dissolution product and has reaction: time, temperature, and potassium concentration. been observed in both laboratory experiments and natural The S-I reaction is of special signifi cance because the extent mineral assemblages. This material is largely amorphous, of the reaction, termed “smectite illitization,” is associated with particle sizes in the nanometer range. Other biogenic with a specifi c combination of temperature and time. These minerals include pyrite, siderite, and vivianite. A mineral same conditions can trigger maturation, migration, and assemblage of quartz, pyrite, and calcite has been used to recognize the role of microbes in mediating mineral reac- tions in ancient marine sediments and in regulating global Si and Fe fl uxes (Vorhies and Gaines 2009). Microbial Formation of Clay Minerals Clay minerals are common weathering products at low temperatures and neutral to acidic pH. Therefore, it is common to fi nd that microbes are involved in the process of rock weathering and clay formation. In fact, microbially catalyzed rock and mineral weathering rates can be orders of magnitude higher than the chemical equivalent, espe- cially when rocks and minerals contain nutrients such as phosphorus, a limiting nutrient in microbial metabolism (Rogers and Bennett 2004). Fisk et al. (2006) showed that microbial weathering of mafi c silicates, basalts, and glasses produces many varieties of clay minerals, such as smectite, , and serpentine. Typically, microbes do not precipi- tate clay minerals directly, but the products of their weath- Schematic diagram showing a typical 2:1 structure of FIGURE 2 a clay mineral such as nontronite (an iron-rich smec- ering reactions reprecipitate to form clay minerals when tite) and microbial reduction of structural Fe(III). Si and Al are conditions become favorable. Reactive sites on bacterial tetrahedrally coordinated and Fe(III) is octahedrally coordinated. surfaces can promote nucleation. Indeed, poorly crystalline The octahedral layer is sandwiched between two tetrahedral layers, clay minerals are commonly observed as surface coatings forming a 2:1 structure. The bioreduction of octahedral Fe(III) is coupled with the oxidation of lactate to acetate. Electron transfer is on microbial cells (Konhauser 2006). Upon aging, the shown to take place parallel to the clay layers, but this does not primary precipitates on bacterial fi laments and cell walls exclude other possibilities. DRAWING COURTESY OF DEB JAISI WITH MODIFICATIONS

ELEMENTS 114 APRIL 2012 A B

(B) platy illite from the Rotliegend of northern Germany. IMAGES FIGURE 3 Scanning electron microscope (SEM) images of (A) (a member of the smectite family) COURTESY OF THE IMAGES OF CLAY ARCHIVE OF THE CLAY MINERALS SOCIETY coating detrital grains in Miocene arkose, Madrid Basin, Spain, and (WWW.MINERSOC.ORG/PAGES/GALLERY/CLAYPIX/INDEX.HTML) are likely transformed into crystalline clay minerals. In structural Fe(III) causes small and fully reversible changes this process, extracellular polymeric substances can serve in the structure and chemistry of the clay mineral. Other as a template for clay mineral synthesis. studies have observed reductive dissolution (Dong et al. 2009; Stucki 2011). It is now clear that both mechanisms Microbial Reduction of Fe(III) in Clay Minerals operate and that the relative importance of one versus the and Its Effects on Their Physical and other depends on many factors, including the nature of Chemical Properties the clay minerals (i.e. iron content, layer charge, and crystal Iron is the fourth most abundant element in the Earth’s chemistry), the extent of reduction, the chemistry of the crust and occurs in all clay minerals (Moore and Reynolds aqueous medium, and the type and nature of the micro- 1997; Stucki 2006). Clay minerals often account for about organisms. Among these, the extent of reduction appears half the iron in soils and sediments. Much of the structural to play an important role. When the extent of reduction iron in clay minerals is ferric iron, which can be reduced is small (<30%), the smectite structure remains stable, but either chemically or biologically. In a typical bioreduction above this threshold, it becomes unstable and the clay experiment, structural Fe(III) in clay minerals serves as an mineral may dissolve, with the formation of secondary electron acceptor, and organic matter acts as an electron mineral phases such as amorphous silica, siderite, vivianite, and illite, depending on the specifi c experimental condi- donor in either a nongrowth or growth medium (FIG. 2). After a few weeks, the color of the solution changes to tions (Dong et al. 2009 and references therein). deeper green in the experimental tubes (FIG. 4A) indicating The reduction of structural Fe(III) to Fe(II) tends to decrease reduction of Fe(III) to Fe(II). Iron-reducing bacteria typi- the surface area, interlayer spacing, water swellability, and cally attach themselves to clay mineral surfaces during hydraulic conductivity of clay minerals. In general, reduc- bioreduction (FIG. 4B, C). tion increases the negative layer charge and cation exchange To date, a wide range of bacteria and archaea have been capacity (Stucki and Kostka 2006; Stucki 2011), while the used to reduce structural Fe(III) in clays (Dong et al. 2009; interlayer cations become less exchangeable. These physical Liu et al. 2011; Bishop et al. 2011). In general, methanogens and chemical changes of clay minerals would have are less effi cient in reducing structural Fe(III) than iron- profound effects on soil fertility and contaminant mobility. reducing and sulfate-reducing bacteria. Smectites have For instance, a decrease in the reactive surface area and been shown to be more reducible than other clay minerals, the associated collapse of smectite layers would decrease likely due to their high layer expandability, low layer the adsorption capacity of nutrients and even trap some charge, and high surface area (Dong et al. 2009). nutrients (such as K and ammonium) in the smectite inter- layer that would otherwise be available to plants. To over- Multiple factors infl uence the rate and extent of Fe(III) come this problem, farmers may need to apply fertilizer bioreduction. The most important are the microbe/clay more frequently to maintain a constant crop yield. ratio, the clay mineral surface area, the chemistry of the Similarly, reduced smectites can more effi ciently degrade aqueous medium, the presence or absence of electron- pesticides, thus making them less effective in killing pests shuttling compounds, and temperature (Dong et al. 2009). (Stucki and Kostka 2006). An alternative approach that Even under ideal conditions, not all structural Fe(III) in mitigates these adverse effects is for farmers to till their clay is biologically reducible, likely due to an inhibition agricultural lands, thus reoxidizing the reduced soils. effect of biogenic Fe(II) that may be released during reduc- Tilling soils has probably been practiced for thousands of tive dissolution of clay and then sorbed onto clay and years, but farmers may not be fully aware of this redox bacterial surfaces. The sorbed Fe(II) may block electron effect! The purpose of tilling and plowing is essentially to transfer and hinder further bioreduction. This inhibition reoxidize structural Fe(II) in reduced smectite. However, effect may be alleviated by removing Fe(II) from clay and reoxidation does not restore all the physical and chemical bacterial surfaces through dynamic fl ow of the aqueous properties, and some of the changes are permanent (Stucki solution. The incomplete reduction of structural Fe(III) by and Kostka 2006). With multiple cycles of reduction and microorganisms may also be caused by inhibition due to oxidation, soil properties may deteriorate to a point where the accumulation of solid products on reactive clay and soil fertilization is increasingly needed. Because of the cell surfaces or by change to the energetics of the system predominance of clay minerals in soils and their recyclable (Dong et al. 2009). nature, the deterioration of soil properties is primarily due to clay mineral redox cycling. What happens to the clay mineral structure and chemistry during and after Fe(III) bioreduction is a matter of debate. Several studies have reported that bacterial reduction of

ELEMENTS 115 APRIL 2012 anite, depending on the chemistry of the solution. This B microbially catalyzed S-I reaction took place in the labora- tory at room temperature and pressure in 2 weeks, in contrast to the slow abiotic reaction rates in either a labora- A tory simulation system (250–350 °C, 50–100 MPa, for 4–5 months) (Huang et al. 1993) or in the natural environment (Pevear 1999). Subsequent experiments under geologically more realistic conditions have expanded these initial results. The pres- ence of organic matter favors microbial mediation of the S-I reaction (Dong et al. 2009). Anaerobic, thermophilic (65–68 °C), metal-reducing bacteria isolated from the deep C subsurface were found to have the same ability as meso- philic bacteria in promoting the reaction under favorable conditions (alkaline pH, external supplies of Al and K) (Dong et al. 2009). Even sulfate-reducing bacteria and methanogens are capable of promoting the reaction. These results show that several types of microbes are capable of promoting this important mineral reaction under diage- netic conditions. All these previous experiments used nontronite to study the role of microbes in the S-I reaction. Nontronite, an iron-rich smectite, is not a typical clay mineral in soils or FIGURE 4 (A) A typical iron-bioreduction experimental setup. In the absence of O2, iron-reducing bacteria are forced recent sediments; instead, beidellite and montmorillonite, to reduce structural Fe(III) to Fe(II), thus changing the color of the both iron-poor smectites, are more typical. Nonetheless, suspension. The left tube is the abiotic control, and the right tube is the biotic treatment with Shewanella oneidensis MR-1. The tubes are these compositions all contain structural Fe, and structural approximately 20 cm long. (B) SEM image showing the attachment Fe in smectites in general is assumed to behave like Fe in of MR-1 cells onto ferruginous smectite during reduction of struc- nontronite. Under this assumption, recognition of the tural Fe(III). FROM DONG ET AL. (2003), REPRODUCED WITH PERMISSION FROM microbial role in promoting the S-I reaction is important THE CLAY MINERALS SOCIETY (C) SEM image showing the attachment of for multiple reasons. First, this microbially mediated S-I the thermophilic methanogen Methanothermobacter thermautotro- phicus on nontronite during its reduction of structural Fe(III), in a reaction provides an example of the catalytic effect of culture medium under anaerobic conditions at 65 °C and neutral microbes in mediating certain geological processes; this pH. PHOTO COURTESY OF JING ZHANG recognition is in some sense comparable to the discovery of the microbial role in promoting dolomite precipitation Iron reduction may also exert a benefi cial effect. One (Vasconcelos et al. 1995). Second, the microbially catalyzed example is decreased contaminant mobility if, after struc- S-I reaction provides a physical basis and mechanism for tural Fe(III) reduction, contaminants are trapped inside refi ning the smectite illitization model, with possible impli- the interlayer and thus become less exchangeable. For the cations for petroleum exploration (Huang et al. 1993). purpose of remediation, iron reduction can be accelerated Third, when coupled with microbial measurements, this by injecting certain microbes or nutrients into the soil to newly recognized model offers an explanation of why the stimulate indigenous microbes (Stucki et al. 2007). S-I reaction occurs in certain modern sediments under low temperature and pressure (Kim et al. 2004). The microbi- Microbial Oxidation of Fe(II) in Clay Minerals ally catalyzed S-I reaction has even been proposed to have Microorganisms can also oxidize structural Fe(II) in clay occurred in ancient marine sediments, in which the reduc- minerals, but the mechanisms and controlling factors are tion of structural Fe(III) dissolved smectite and formed poorly understood. Shelobolina et al. (2003) have shown biogenic minerals such as quartz, pyrite, and carbonates that the oxidation of structural Fe(II) in smectite by (Vorhies and Gaines 2009). Fourth, dramatic changes asso- Desulfi tobacterium frappieri is coupled with the reduction ciated with the S-I reaction would signifi cantly affect the of nitrate, which has implications for removing nitrate physical and chemical properties of soils and sediments; contamination from the environment using reduced clay thus, it is important to understand the rate and extent of minerals. Limited data indicate that, compared with chem- this reaction when designing strategies for maximizing ical oxidation of structural Fe(II) by nitrate alone or by air, nutrient retention and minimizing contaminant mobility. the rate of microbially mediated, nitrate-dependent Fe(II) Fifth, the illitization of smectite, a major component of oxidation appears faster (Yang 2010). used in radioactive waste disposal, releases water and leads to changes in hydraulic conductivity (Mulligan The Microbially Mediated Smectite-to-Illite et al. 2009). This change would have a major effect on the Reaction stability of used for high-level radioactive waste disposal and could potentially result in the failure of waste Although the importance of the S-I reaction has long been canisters (Perdrial et al. 2009). recognized, the role of microbes in promoting this reaction was only recently demonstrated (Kim et al. 2004). Under favorable conditions, the iron-reducing bacterium ENVIRONMENTAL APPLICATIONS Shewanella oneidensis MR-1 can reduce structural Fe(III) in Redox-manipulated clay minerals have a wide range of nontronite to Fe(II) and partially dissolve the nontronite. applications. Below, I highlight a few examples for envi- Upon recombination of the dissolved constituents, illite ronmental remediation. precipitates from the aqueous solution (FIG. 5). Because of compositional differences between nontronite and illite, Heavy Metal Remediation Using Redox- the dissolution of one unit of nontronite does not make Manipulated Clay Minerals one unit of illite. More likely, the dissolution of multiple There are several mechanisms for the remediation of heavy units of nontronite precipitates one unit of illite, with metals by clay minerals. One classical strategy is adsorption excess Si and Fe precipitated as silica and siderite or vivi- and absorption, which take advantage of the high external

ELEMENTS 116 APRIL 2012 reduction of structural Fe(III) in chlorite (Zhang et al. 2009), with the implication that Fe(II) in nontronite may not reduce and immobilize U(VI). Organic-Contaminant Degradation In addition to heavy metal remediation, reduced smectites have been found to be effective in degrading organic compounds, including pesticides, 2,4,6-trinitrotoluene, nitroaromatics, carbon tetrachloride, chlorinated and nitroaliphatic compounds (Stucki and Kostka 2006 and references therein; Fialips et al. 2010). Because reduced smectites remove these compounds from aqueous solution much faster and to a greater extent than their oxidized counterparts (supposed to have similar surface area and adsorption capacity), the removal mechanism appears to be by degradation. The detection of various degradation products further supports such a mechanism.

FIGURE 5 Transmission electron microscope image showing the microbially catalyzed smectite-to-illite reaction. A thick Advantages of Microbially Mediated Clay packet of illite layers (each 1.0 nm thick) formed in the matrix of Minerals in Remediating Inorganic and smectite (1.3 nm thick layers). The selected area electron diffraction patterns show a diffuse ring pattern for smectite and discrete Bragg Organic Contaminants refl ections for illite. FROM KIM ET AL. (2004), REPRODUCED WITH PERMISSION Coupled with microbial activity, clay minerals exhibit FROM THE AMERICAN ASSOCIATION FOR THE ADVANCEMENT OF SCIENCE certain properties that can be explored for waste disposal. First, iron-bearing clay minerals help establish the phys- and internal surface area of clay minerals. Although this ical/hydrogeological conditions of redox transition zones strategy may be effective in the initial removal of heavy because of their small size and limited hydraulic conduc- metals, it may not be permanent because these inorganic tivity. Because typical clay minerals in soils and sediments, contaminants can be remobilized if the environmental such as smectite, provide a solid-phase reservoir of Fe(III) conditions change. Other strategies involve the coprecipita- and Fe(II) (3–5% total iron, with the ferric/ferrous ratio tion of metals and radionuclides into clay mineral struc- depending on redox state; Stucki 2006), they can buffer tures (Brandt et al. 2007). This strategy may be more the redox conditions through the transition zone and mini- “permanent” as clay minerals are fairly stable under a wide mize any chance of reoxidizing reduced heavy metals and range of conditions. radionuclides. A more recent approach is redox manipulation facilitated Second, because iron redox cycling largely occurs in the by microbes. It is assumed that Fe(II) in smectite, possibly solid state, especially when the extent of cycling is small, produced via the biological reduction of structural Fe(III), Fe(III) produced from the reduction of heavy metals or the reduces oxidized forms of heavy metals, such as Tc(VII), degradation of organic compounds can be recycled back according to the following general reaction (Jaisi et al. to Fe(II), generating a renewable source of electrons. 2009): Methods have been discovered for the in situ reduction of Fe(III) within soil or sediments by stimulating indigenous structural Fe(II) + Tc(VII)  structural Fe(III) + Tc(IV) . Fe-reducing bacteria through the addition of a carbon source and an electron donor, such as ethanol or glucose A number of studies have examined the interactions of (Stucki et al. 2007). clay-associated Fe(II) with heavy metals and radionuclides, including Tc (Jaisi et al. 2009; Bishop et al. 2011), U (Zhang Third, because of low permeability and rapid particle aggre- et al. 2009, 2011), and Cr (Taylor et al. 2000). Even when gation, clay minerals are ideal matrices to immobilize excess Fe(II) is available in an experimental protocol, not metals and radionuclides for long-term disposal. Secondary all Fe(II) is reactive. Fe(II) reactivity depends on the crystal- contamination can be minimized because of low oxygen chemical environment of Fe(II) in clay minerals. For penetration (Jaisi et al. 2009). Tc(VII) reduction, Fe(II) in smectite is the most reactive, and Fe(II) in illite the least (Bishop et al. 2011). Differences OUTLOOK in surface area, surface charge, layer expandability, and layer charge between smectite and illite are important Despite the past 20 years of research, challenges and many factors in accounting for this difference (Bishop et al. 2011). unanswered questions still remain. Much of our under- For this reason, any transformation of smectite to illite has standing of microbially mediated clay mineral transforma- an adverse effect on metal reduction and immobilization. tion is qualitative. It is still poorly known to what extent Conversely, any method to reverse the S-I reaction would these mineral reactions are mediated by microbial activity be of benefi t. Not only does smectite reduce and immobi- in nature. What is the relative importance of abiotic versus lize Tc(VII), but the reduced Tc(IV) resides inside the biotic effects in mineral evolution? How have clay–microbe mineral matrix, minimizing the potential for remobiliza- interactions evolved through geological history? To what tion (Jaisi et al. 2009). extent do such interactions contribute to ocean chemistry and atmospheric composition? Reduced structural Fe(II) in smectite is an effective reduc- tant for Cr(VI) as well. Sorption of Cr(VI) onto a clay Our knowledge of microbe–clay interactions is largely mineral surface appears to be a prerequisite for subsequent derived from laboratory experiments that are greatly reduction. Unlike Tc(VII) and Cr(VI), U(VI) reduction by simplifi ed relative to what happens in nature. For example, clay-associated Fe(II) is kinetically slow. For some clay typical bioreduction experiments use pure microbial minerals, such as nontronite, redox chemistry may favor cultures and pure clay minerals in a defi ned buffer or the oxidation of U(IV) by Fe(III), which is opposite to the medium, mostly at room temperature and pressure, in static direction of the Tc(VII) reduction reaction. Because of the batch reactors. However, in nature, microbes exist in rapid oxidation of U(IV) by structural Fe(III) in nontronite, communities, and they may cooperate or compete in their uranium can serve as an electron shuttle for microbial interaction with minerals. Furthermore, several clay

ELEMENTS 117 APRIL 2012 minerals may be present, often mixed with various Fe mineral redox manipulations impact aquifer porosity and oxides and other silicates. Aqueous media such as ground- permeability and, subsequently, metal transport behavior? water aquifers are often complex, with various types of Would clay minerals enhance, rather than retard, metal organic matter present. Natural systems are usually transport? dynamic, with varying rates of fl ow. How can laboratory- based results be extrapolated to complex fi eld applications? As interest in this fi eld is growing, we can anticipate that What possible issues are involved in spatial and temporal answers to these questions will be forthcoming. Certainly scaling? These questions are especially relevant to the there are many opportunities and challenges facing microbially catalyzed S-I reaction model, as it is not yet researchers who are dedicated to studying clays and clear how widely this model is applicable to the overall microbes. I hope that this review will encourage collabora- picture of clay diagenesis. The laboratory-optimized condi- tion among clay mineralogists, soil scientists, microbiolo- tions may be satisfi ed only in certain geological environ- gists, and environmental engineers. ments. The lack of these conditions may be the reason why smectite in soils and sediments persists despite the presence ACKNOWLEDGMENTS of active microbial processes (mostly non-iron-reducing I am grateful to the many students and colleagues who activity). Likewise, illite in modern sediments is mostly have allowed me to share the joy of their discoveries. To derived from the erosion of sedimentary rocks and is not Jinwook Kim, Deb Jaisi, Dennis Eberl, Gengxin Zhang, necessarily biogenic in origin. Future studies should focus Michael Bishop, Deng Liu, Jennifer Seabaugh, Junjie Yang, on the identifi cation of these conditions in natural settings Jing Zhang, Timothy Fischer, Linduo Zhao, and others, and quantitatively assess the relative importance of the I extend my thanks for their contributions to this effort. biotic versus abiotic effects on the S-I reaction. This work was supported by grants from the National Basic Reduced smectites have shown great promise in contami- Research Program of China (973 Program) (2012CB822004), nant remediation. Although the degradation of organic the National Science Foundation of China (41030211), and compounds by reduced smectites has been well established, the U.S. Department of Energy (DE FG02-07ER64369 and the application of reduced smectites to heavy metal and DE-SC0005333). I am grateful to James Drever, Peter radionuclide remediation is at an early stage. How can such Heaney, and an anonymous reviewer, whose comments a strategy be implemented at the fi eld scale? How do clay improved the quality of the manuscript.

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