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Environmental Selenium Research: From Microscopic Processes to Global Understanding Lenny H. E. Winkel,*,†,‡ C. Annette Johnson,† Markus Lenz,§,∥ Tim Grundl,⊥ Olivier X. Leupin,# Manouchehr Amini,† and Laurent Charlet▼ †
Eawag, Swiss Federal Institute of Aquatic Science and Technology, Ueberlandstrasse 133, P.O. Box 611, 8600 Duebendorf, Switzerland ‡ Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Sciences, Swiss Federal Institute of Technology (ETH) Zurich, 8092 Zurich, Switzerland § University of Applied Sciences and Arts, Northwestern Switzerland (FHNW), Institute for Ecopreneurship, School of Life Sciences, Gruendenstrasse 40, 4132 Muttenz, Switzerland ∥ Sub-Department of Environmental Technology, Wageningen University, 6700 EV Wageningen, The Netherlands ⊥ School of Freshwater Sciences and Department of Geosciences, University of Wisconsin−Milwaukee, 3209 North Maryland Avenue, Milwaukee, Wisconsin, United States # Nagra, Hardstrasse 73, 5430 Wettingen, Switzerland ▼ ISTerre, Institute of Earth Sciences, University of Grenoble, CNRS, P.O. Box 53, 38041 Grenoble Cedex 9, France Nevertheless, recently, concern has been raised about possible adverse health effects of high Se intake in humans (>75 μg per day), including an increased risk of diabetes.11 At very high daily doses (>400 μg per day), Se is acutely toxic, whereas chronic exposure of subacute concentrations can lead to brittle hair and nails, skin lesions, and neurological disturbances in humans.12 Selenium toxicity in both humans and animals, for instance, has been reported in the Chinese provinces Hubei and Shaanxi and in Punjab (India), where Se levels in locally produced foods where found to be very high (750−4990 μg per person and day7). In Punjab, but also elsewhere, it has been argued that irrigation in combination with high evaporation rates is largely responsible for excess Se in the irrigated soils and food crops13 (Figure 1). The variation of Se status in humans largely depends on the diet. Plant foods are the major dietary sources of Se in most countries around the world, followed by meats and seafood (http://ods.od.nih.gov/factsheets/selenium/). The Se contents of agricultural soils show substantial geographical variations14 and so do the foodstuffs that were nourished by these soils. To prevent future health hazardsboth related to Se excess and deficiencyit is essential to understand the factors controlling the dynamic distribution of Se in the environment. In this feature we will describe how the latest development of analytical methods will result in an improved knowledge of the mechanisms that control the geochemical behavior of Se in the surface environment. New techniques and methods enable accurate and precise Se measurements at lower concentrations and are therefore ideal for environmental studies. We will highlight how an advanced understanding of the prevailing geochemical mechanisms on a microscopic scale will pave the way for largescale predictions of Se distribution and bioavailability in the environment.
T
he essential trace element selenium (Se) plays a fundamental role in human health. It is a component of several major metabolic pathways including thyroid hormone metabolism, antioxidant defense systems, and immune function.1 In humans, selenium has one of the narrowest ranges between dietary deficiency (400 μg per day).2 International agencies have therefore set dietary reference values in the range of 30−55 μg per day for Se intake.3 Insufficient Se supply has been associated with growth retardation and impaired bone metabolism4 and is thought to cause abnormalities in thyroid function.5 In central China and South East Siberia, very low Se contents of locally produced food have been related to geographically widespread endemic diseases, such as Keshan disease (a cardiomyiopathy) that was first recognized to be related to Se deficiency in 1935, or the chronic, degenerative osteoarthrosis Kashin Beck disease.6 Daily intake in affected areas ranges from only 7 to 11 μg per person per day.7 On a global scale it is estimated that 0.5−1 billion people are directly affected by Se deficiency.8 In general, areas low in natural Se are more widespread and extensive than areas with excess levels of Se. Set against this, Se does appear to have a role in strengthening the immune system1,9 and can detoxify As[III] and Hg[II] by forming species with covalent As−Se and Hg−Se bonds.10 © 2011 American Chemical Society
Published: November 30, 2011 571
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Figure 1. Schematic global cycle of Se with main focus on the terrestrial environment. Blue arrows indicate processes that involve oxidation of Se species and green arrows indicate processes that involve reduction of Se species. Warning symbols indicate specific environmental settings that are at risk of either developing Se deficiency (open warning symbol) or Se excess (shaded warning symbol).
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can occur as the oxyanions selenate (SeO42−) or selenite (HSeO3−). At circumneutral pH values (between 6.5 and 7.5) and highly oxidizing conditions (Eh values of ∼400 mV or more) selenate is thermodynamically favored. Selenate is not particularly prone to sorption. It does form easily reversible surface complexes on clay minerals, however, competition with sulfate for sorption sites enhances its mobility.26 Alkaline pH values and high redox potentials favor Se bioavailability to plants. Selenite is stable under moderately oxidizing to reducing conditions (down to Eh values of ∼0 mV). Selenite is far more subject to irreversible sorption to iron oxides,27 the edges of clay minerals,28 and soil organic matter29 than selenate. This affinity for sorption reduces Se availability for plant uptake in soils with high levels of iron oxides, clays, or soil organic matter. It should be pointed out, however, that plant Se accumulation can vary by more than 2 orders of magnitude at a given soil Se concentration among different plant taxa (reviewed in Bitterli et al.30). Because factors distinct from total concentrations determine Se content in food and feed plants, the classical definitions of deficient (0.5 mg total Se per kg) soils16 may be, at least for some cases, misleading. It is the bioavailability of Se, and thus the speciation, in soils that needs to be considered. Furthermore, a large amount of organic matter can lead to reducing conditions where both biotic31 and abiotic mechanisms32 lead to the formation of elemental selenium (Se[0]) or metal selenides (Se[−I]/[−II]). Elemental Se is not soluble in water and is classified as unavailable to biota.
NATURAL FACTORS THAT INFLUENCE SELENIUM DISTRIBUTION AND BIOAVAILABILITY The global Se distribution (i.e., the dynamic distribution that may change over time) is mainly determined by natural sources and transport processes (see Figure 1). Soils can contain highly variable Se contents varying from below 0.01 mg per kg in Sedeficient soils, up to 1200 mg per kg in Se-rich soils15,16 Seleniferous soils are often located in relatively small hotspots derived from Se-rich rocks, such as black shales, carbonaceous limestones, carbonaceous cherts, mudstones, and seleniferous coal,17−19 or result from irrigation with Se-rich waters.13 The contamination of irrigation drain water and subsequently of surface waters in the San Joaquin Valley of California (United States),20,21 and of soils in Punjab (India)22,16 are examples of Se enrichment via water/rock interaction and irrigation with Se-rich groundwater, respectively. Apart from terrestrial environments, marine environments are an important source of Se via transfer to the atmosphere, and the atmosphere is in turn a significant source of Se for the terrestrial environment.23,24 An extensive review on atmospheric selenium and transfer processes has been published by Wen and Carignan.24 Areas with adequate or deficient Se soils are present at much larger scales than areas where Se excess prevails. It is important to note that it is not primarily the Se content in the soils that is responsible for Se uptake in plants and organisms, but rather the bioavailability to plants and organisms, which dictates the entrance of Se in terrestrial food chains. For instance, studies of Chinese soils in Keshan disease areas showed that soil Se levels are low (average 0.15 mg per kg Se), but not critically low, i.e., sufficient according to the classical definition of deficient (0.5 mg total Se per kg) soils.16 In those areas, Se deficiency was thus rather caused by immobilization of Se by soil organic matter (via adsorption and/or (bio)chemical reduction) than by low total Se levels.25 Selenium bioavailability is a result of the interplay among prevailing geochemical parameters, i.e., pH and redox conditions, and soil properties, such as organic carbon, Fe hydroxide, and clay contents, and Se speciation. Selenium exists in the environment in five metastable oxidation states: (−II), (−I), (0), (+IV), and (+VI).15 In oxidizing environments Se
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BIOAVAILABILITY OF ELEMENTAL SE: THE NANO EFFECT In contrast to elemental sulfur,33 elemental Se has a large stability region and is thus thermodynamically favored in many natural environments. It has even been proposed that elemental Se represents one of the largest pools of Se in aquatic systems, accounting for about 30−60% of total Se in sediments (Zhang et al.34 and references therein). In nature, the reduction of water-soluble selenite and selenate to elemental Se is largely controlled by microbially mediated processes, both of dissimilatory (i.e., respiratory) and nondissimilatory manner35 but also by surface-mediated reduction 572
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processes.36 The ability to reduce Se oxyanions to so-called biogenic elemental Se (BioSe) is widespread in the microbial environment.37 BioSe, irrespective of its microbial origin, is usually found as spherical particles in the nanometer range (average ∼300 nm,38 yet at times considerably smaller39 or larger40) either intra- or extracellularly.38 In the aquatic environment, BioSe can remain in colloidal suspension for weeks.34 If exposed to oxygenated zones of water bodies it may be subject to reoxidation processes, resulting in the formation of selenite and selenite that are again bioavailable. Due to the higher surface to volume ratio, the kinetic of reoxidation is likely to be faster in nanosized Se in contrast to Se with larger particle sizes. Nanosized Se in the range of a few nanometers only, whether biogenic or formed by surface-mediated reduction, may even directly enter cells, as found for other nanomaterials.41 Thus, the classification of elemental Se as being bio-unavailable can be deceptive when it comes to nanosized particles. The apparent reason for the tendency of BioSe to form spherical, nanometersized particles is the presence of an organic polymer layer consisting ofbut not exclusivelyproteins42,43 of microbial origin. For other chalcogenide biogenic nanoparticles (i.e., ZnS), it has been demonstrated that it is this proteic fraction associated that limits their dispersal in the environment.44 It can be anticipated that due to the particular properties conferred by the proteic fraction associated (e.g., different hydrophilicity and/or surface potential) and the nanometer size, BioSe will distribute differently than larger elemental Se particles not having such associations in the environment. One can easily imagine that a dissociation or degradation of the organic fraction in certain environments may occur, changing the distribution of the entire composite BioSe (i.e., elemental Se + organic molecules associated). However, this has not been studied so far under environmental conditions. Upon demonstration that BioSe shows a particular distribution and/ or bioavailability in contrast to bulk elemental Se, a reevaluation of current risk assessment data in elemental Se-rich soils (and sediments) will be necessary.
systems could be biased, e.g., by inhibition/toxicity to microbial communities or changes in transport behavior caused by precipitation of insoluble phases. Only state-of-the-art analytical instrumentation offers a sufficiently high sensitivity to ensure this transferability, particularly in Se-deficient systems.
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LIQUID AND GAS PHASE SPECIATION Knowing the total Se content is only the first step in the assessment of the Se status of soils and other environmental compartments. As outlined before, individual Se species behave fundamentally different in the environment and it is thus crucial to determine Se speciation appropriately. This task requires methods that are not only outstanding in sensitivity but also truly species specific. Furthermore, these methods should prevent any changes in the original speciation during sample preparation and measurements or should have the possibility to derive the original speciation from measured speciation (see e.g., Winkel et al.51). To achieve high sensitivity and low matrix interferences, historically “speciation” methods have vastly made use of hydride generation for the determination of Se species. These methods are based on the assumption that volatile hydrides are formed selectively from one species only (i.e., selenite), so that nonhydride forming species can be determined after conversion to the latter by difference. However, diverse limitations (e.g., incomplete conversion to hydride forming species, suppression of hydride formation by interferences, species loss,52 presence of species apart from selenite, and else) can hamper the latter methodology. Therefore, at least part of the very early speciation work (relying exclusively on hydride generation) might be influenced by these potential sources of bias. To date, many truly species-specific speciation methods with high sensitivity are at hand, mostly achieved by coupling a chromatographic separation with element-specific detection. Most frequently, ICP-MS detection is coupled to liquid chromatography (LC), using retention times of known standards for identification and quantification of species. Great care has to be taken to ensure that the original sample speciation is maintained, in particular when sample pH is adjusted to match the LC eluent used.53 To complicate matters, it appears that Se liquid- and gas-phase speciation can become increasingly complex when Se is converted during biological processes due to the formation of a large number of organo−Se compounds.54 In these cases, it might not always be possible to find the appropriate standard matching the retention time of the unidentified species. State-of-the-art mass spectrometry nowadays offers a mass resolution that is high enough to identify unknown compounds even without mandatory matching to standards55 (Figure 2). We therefore believe that coupling of LC-ICP-MS speciation approaches (for separation and quantification) with high-resolution tandem MS (for identification) will play an essential role in future research concerning the fate of Se in the environment. Another emerging area of study is the terrestrial (and marine) biotic Se alkylation, i.e., the transfer of organic groups (methyl, ethyl, etc.) to Se atoms. Alkylation processes are thought to be major processes in the biogeochemical cycle of Se (see Figure 1).56−58 Because these processes result in the formation of volatile compounds, on the one hand they might enhance Se deficiency in soils and plants, but on the other hand could also lead to increased atmospheric transport of Se and deposition elsewhere. Also here, the challenge is to quantify such Se species specifically and at trace concentrations of
