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1 X-RAY SPECTROMICROSCOPY A Tool for Environmental Sciences High spectral and spatial resolution makes synchrotron-based spectromicroscopy well suited for environmental applications. JÜRGEN THIEME UNIVERSITY OF GÖTTINGEN (GERMANY) IAN McNULTY STEFAN VOGT ARGONNE NATIONAL LABOR ATORY DAV ID PATERSON AUSTR ALIAN SYNCHROTRON Environmental science is an extremely diverse field that impacts many facets of science, industry, and everyday life. Because of the complexity of environmental processes and the many mutual interactions involved, competence is required in more than one area of expertise, and a multidisciplinary approach is often necessary. The experts in geochemistry, hydrology, microbiology, and atmospheric and soil sciences, to name a few, are essential in this regard. For example, the complex roles of carbon, nitrogen, phosphorus, and sulfur cycles in the environment are incompletely understood, as are their mutual interactions. Similarly, our knowledge of uptake and metabolism of environmental contaminants by biological organisms is far from complete. Elemental transport, redox reactions, microbial activity, and anthropogenic influences all affect these processes. Knowledge of each individual piece of the puzzle contributes to a better understanding of the overall picture American Chemical Society October 15, 2007 / Environmental Science & Technology n 6885
2 X-ray spectromicroscopy is a powerful tool for addressing key questions in the environmental sciences, because of its high spectral and spatial resolution. It has been used successfully in the fields of materials research and biology and recently in environmental studies for example, in the form of micro-x-ray fluorescence and spectromicroscopy with a spatial resolution <100 nm (1, 2). The combination of high-resolution microscopy with spectroscopic capabilities allows one to determine elemental composition as well as chemical speciation and to identify trace elements on length scales extending to the nanoscale. To define the most important problems and research directions in environmental science for which X-ray spectromicroscopy methods could be indispensable and could have the greatest impact, an all-day workshop was held on May 4, 2006, as part of the 2006 users meetings for the U.S. Department of Energy Office of Basic Energy Sciences user facilities at Argonne National Laboratory. Fourteen speakers, primarily from the environmental sciences fields, presented their latest research and techniques to an enthusiastic audience. The primary aim was to bring together experts in all fields of the environmental sciences to formulate and discuss key issues. A secondary aim was to improve accessibility to X-ray spectromicroscopy methods for environmental science researchers. The workshop scope was limited to an X-ray energy range from the K-absorption edge of carbon (~0.28 kev) to that of iron (~7.2 kev) and to spatial dimensions from the scale of a few micrometers to the nanoscale. The discussion throughout this article will be limited to this energy range; it will cover many environmentally important elements (Table S1 in Supporting Information) and will focus on research that requires submicrometer spatial resolution. Currently, more than a dozen X-ray microscopy stations are operational worldwide. Table S2 in Supporting Information gives a nonexhaustive list of instruments that are capable of spatial resolution <1 µm. In this article, we review some of the results of the workshop, including an evaluation of outstanding problems in environmental science that could serve as a road map for research activities worldwide. Soil colloids imaged in X-ray fluorescence mode using signals from sulfur (red), aluminum (blue), and silicon (green) are shown in the opening art on p The bottom right image is an overlay of the three other images. The green image clearly shows silicon skeletons from diatoms. (Adapted with permission from Ref. 14.) Open questions in environmental sciences The workshop attendees identified a long list of open questions in environmental sciences that X- ray spectromicroscopy might be able to answer. One of the key scientific problems is the speciation of contaminants in natural environmental materials, including the effects of biota on redox transformations of contaminants, sequestration, and mobilization. Because of the high heterogeneity of soils on every length scale, the findings of synchrotron radiation research (at the microscale) need to be related to the much larger scale of actual fields (3). Another topic of great interest is the complex interactions of living and nonliving components of environmental systems. For example, with synchrotron radiation, the formation of minerals inside and near single bacterial cells can be probed, or the role of colloid-mediated environmental processes in natural aquatic systems can be studied. Complex bio-organo-mineral assemblies are involved in these interactions; structures and composition of these assemblies are highly variable and evolve with changes in physicochemical conditions (4). To understand the processes, these assemblies must be studied. Studies of living systems within the environment highlight the topic of scale, from purified proteins to cell cultures to intact organisms, such as plants (5). Sulfur is an element that is straightforward and informative to study because it is ubiquitous and shows many oxidation states, but other elements, such as phosphorus or chlorine, can be measured with X-rays of intermediate energies. For example, spectromicroscopy was used to study ocean phosphorus cycling in sediments overlain by oxic as well as by anoxic bottom water (6). Spectromicroscopy studies can be performed to understand halogen cycles in the environment more fully, especially the fate of chlorine in plants and soils (7). Another area where synchrotron-based research can play an important role is the study of actinide materials, for example, the anaerobic geomicrobial effects on the fate and transport of heavy metals and radionuclides (8). Potential of X-ray spectromicroscopy The spatial resolution achievable with a microscope ultimately is limited by the wavelength of the radiation. The wavelength of X-radiation is much shorter than that of visible light; consequently, a much higher resolution can be achieved with an X-ray microscope. Within the soft X-ray energy range, 13 nm structures have been resolved (9), whereas in the intermediate energy range, the resolution is ~50 nm (10). X-ray microscopy is a very good choice to study colloidal structures in situ, because its penetration depth allows visualization of hydrated samples and its spatial resolution is a good match to the typical sizes of colloids (1 nm to 1 µm). In the so-called water window the energy range between the K-absorption edges of carbon and oxygen photoelectric absorption and phase shift are the two dominating processes of interaction of X- rays with matter. Organic matter, iron oxides, clay particles, and other substances show a much higher X-ray absorption and phase shift than water. As a result, significant natural contrast can be observed in X-ray microscopy of organics in aqueous media, and drying, fixation, and staining of samples are not necessary. The absorption cross section of matter for X-rays in that energy range is much smaller than that for electrons in transmission electron microscopy. The thickness of a water layer at which 0.5 kev X-rays are 6886 n Environmental Science & Technology / October 15, 2007
3 F I G U R E 1 3D computer reconstruction The reconstruction of a tomographic data set of 50 X-ray microscopy images spanning 180 shows the networklike structure of microbially reduced humic substances (left) and the change in appearance to isolated flocks after reoxidation (right). The spatial resolution is ~50 nm. (Images produced in collaboration with John Coates, department of plant and microbial biology, University of California Berkeley.) reduced to 1/e of the original intensity is ~10 µm. By comparison, the intensity of 150 kev electrons is reduced to 1/e with a thickness of only 0.2 µm. As a result, much thicker samples can be penetrated and thus investigated with X-ray microscopy than with electron microscopy. Two types of microscopes are used in X-ray microscopy: the transmission X-ray microscope (TXM), mainly used for imaging, and the scanning X-ray microscope (SXM), mainly used as a microanalysis tool. In both types, Fresnel zone plates typically are used as the high-resolution, X-ray-focusing optic in this energy range. Figure 1 shows an example of a study that uses TXM to investigate the morphological change of formerly anaerobic humic substances after reoxidation (11). The study was performed with the TXM XM-1 at Advanced Light Source (12) in collaboration with John Coates from the department of plant and microbial biology at the University of California Berkeley. The two humic samples were vitrified in glass capillaries, and tomographic data sets were recorded for each sample and then reconstructed. Starting from a network-like appearance in anaerobic conditions, the humics flock together when in contact with oxygen, and larger isolated particles appear. An X-ray microprobe (SXM) is an instrument that can be used to map and quantify element distributions within samples from the environment, as shown in Figure S1 in Supporting Information. Monochromatic X-rays are focused into a spot <1 µm on the sample. An energy-dispersive detector is used to collect the X-ray fluorescence, which is characteristic for each chemical element, emitted from the sample. To create an elemental map, the sample is scanned through the focal spot. The elemental maps in Figure S1 are of a colloidal structure in seepage water from a waste deposit in Germany. Note the heterogeneity of this colloid as well as the obvious twofold structure of it. Although chlorine, potassium, chromium, and iron are more or less ubiquitous, a strong dichotomy exists in the case of manganese or calcium. In an SXM, the polychromatic synchrotron radiation is reduced in its bandwidth to E/ E of ~3000. A detector records the radiation transmitted through the sample. Once the sample is scanned through the focal spot and the transmitted signal is recorded, an image can be generated. Images can be recorded in bright-field, dark-field, or differential-phase contrast mode simultaneously by using configured detectors (13). An additional energy-dispersive detector might collect the fluorescent signal. Because of the scanning process, the time to collect an image usually is longer than with a TXM. However, tuning the wavelength of the incident X-rays yields a spectrum from a specific area of the sample. As the incident X-ray energy is varied, resonances occur that reflect the chemical bonding state of the element as well as steplike change due to absorption of the element. XANES or NEXAFS spectra (both acronyms are used for the same technique) can be seen in Figure S2 in Supporting Information, which shows a spectrum of a mineral-soil horizon taken at the K-absorption edge of sulfur (14). The two peaks in the spectrum represent reduced (left) and oxidized (right) sulfur species. Peak-fitting data analysis can determine the relative amounts of sulfur species present in the sample (15). Advantages of combining microscopy and spectroscopy It is crucial to consider scaling up from the submicrometer world accessible by microscopy to the large field, because heterogeneity exists over a wide range of length scales. To succeed, theorists with statistical and modeling expertise must have good data available, and these results must be connected to standard measurements in other, as well as similar, systems. The phosphorus depletion or enhancement in agricultural soils is one example (16). Environmental sciences strongly interact with bi- October 15, 2007 / Environmental Science & Technology n 6887
4 ology, for example, in the study of biofilms or of biogeochemical pathways in environmental problems. Biological and microbial effects are crucial to most areas of environmental science. Clearly an integrated approach is essential for studying biological as well as other aspects of environmental problems. Metals and metalloids constitute a core interest in the field of environmental sciences; examples are cadmium contamination and uranium remediation. Iron appears to be most prevalent and of broadest interest. XANES spectroscopy is necessary to study reduced and oxidized iron species. Spatially resolved sulfur and phosphorus speciation is important for addressing several problems, such as iron and copper oxidation in soils and the structural organization within mammalian cells. The importance of the role of phosphorus in marine systems is increasingly recognized (6). Organic halogens are of great interest within environmental science, for example, the chlorine speciation in plants. Chlorine and its relation to organic compounds and iron are important. Fluorine and bromine occur in much lower concentrations, and therefore exceptional sensitivity is needed. Experts in synchrotron techniques need more feedback from environmental scientists. Soft X-ray spectromicroscopy has unique capabilities to address complex problems in environmental science. It has the capability of quantitative chemical analysis on a molecular and not just an elemental basis, with quantitation based on high-resolution X- ray absorption or photoelectron spectroscopy. It can be applied to complex materials, including buried interfaces, wet samples (e.g., biological and environmental), and vacuum- and radiation-sensitive materials. X-ray spectromicroscopy combines spectroscopic chemical information with high spatial resolution to provide new research opportunities. For spectromicroscopy, the incident X-ray energy has to be tunable; the spatial resolution should be <100 nm. This is crucial to perform XANES studies of colloidal particles or of submicrometer-sized polyphosphates. The instrumentation must have the flexibility to do fast, wide-range scans as well as slower, high-resolution scans to obtain overview maps of a sample as well as to zoom in on a detailed area of interest. Tomography studies of systems from the environment are highly desirable, for example, to understand transport processes. The energy range of kev seems to cover a very large part of the current research interests. An extension to higher energies (~12 kev) is desired to reach some important transition metals. Radiation damage has to be considered seriously, because many spectroscopy studies are extremely sensitive to such damage. Studying and quantifying radiation damage are regarded as essential to make data and damage thresholds available to the community. Extant X-ray microscopy radiation damage data are helpful but are primarily about structural and not spectroscopic changes. The greatest gains in sensitivity will result from developing better detectors with greater acceptance. It was clear from the workshop that experts in synchrotron techniques need more feedback from environmental scientists. Workshop attendees pointed out that researchers should focus on answering the important questions, as opposed to developing an instrument that has too broad a scope. The challenges are, of course, manifold. Researchers must deal with a vast sample heterogeneity and complexity. Getting fresh samples in the natural state is a major issue, and delicate samples such as actinides are difficult to handle. The state of the sample (aqueous or dry, oxic or anoxic) must be as close to natural as possible. Samples in a cryo state should be manageable. The sample throughput has to be increased to provide the environmental scientist with a quantity of data sufficient for analysis. Currently, one of the limits of the technique is sample preparation, and progress would be better if samples could be viewed more easily in their natural states. The task of the spectromicroscopy experts is to provide good data to theorists with statistical and modeling expertise. Dynamic scaling of systems is another area that begs to be analyzed by theorists. It is crucial to consider the big picture and relationships as pathways, or length scales, to other data and fields. More efficient rapid-analysis tools such as programs for spatial correlation, principal components analysis, or cluster analysis should be available. Heterogeneity exists over a wide range of length scales. The question is how to relate bulk to localized measurements. Standard measurements have to be connected to measurements in similar as well as diverse systems. It is important to use other X-ray methods like SAXS, µsaxs, µxrd, or XMCD as well. In situ studies by micro-ir, micro-raman, or NMR techniques are highly desirable. On-site access to nonsynchrotron tools is important but not at the expense of beam time, and having these ancillary tools nearby is very helpful. Another big challenge is to disseminate the knowledge about X-ray spectromicroscopy as a useful tool to more environmental scientists. Publications in generic environmental journals are a major key to accomplish this. A common complaint of environmental scientists is poor access to the necessary instruments because of oversubscription, which ironically will get worse if dissemination is successful. Access can be improved with better experiment efficiency. Most beam lines are adequate now, but more facilities, more efficient detection, and dedicated instrumentation would help tremendously. An expansion in quality and quantity of the already available techniques is regarded as absolutely necessary n Environmental Science & Technology / October 15, 2007
5 Jürgen Thieme is a scientist at the Institute for X-ray Physics at the University of Göttingen (Germany). Ian McNulty and Stefan Vogt are scientists at Advanced Photon Source, Argonne National Laboratory. David Paterson is a scientist at the Australian Synchrotron. Address correspondence about this article to Thieme at jthieme@gwdg.de. Supporting Information Additional information is available in the form of two tables and two figures, including elemental maps of a colloidal structure in seepage water from a waste deposit in Germany. This material is available for free via the Internet at acs.org. References (1) Aoki, S., Kagoshima, Y., Suzuki, Y., Eds. Proceedings of the 8th International Conference on X-ray Microscopy; Institute of Pure and Applied Physics Conference Series 7, (2) Susini, J., Joyeux, D., Polack, F., Eds. Proceedings of the 7th International Conference on X-ray Microscopy. J. Phys. IV 2003, 104. (3) Manceau, A.; et al. Deciphering Ni Sequestration in Soil Ferromanganese Nodules by Combining X-ray Fluorescence, Absorption, and Diffraction at Micrometer Scales of Resolution. Am. Mineral. 2002, 87, (4) Weber, K.; Achenbach, L.; Coates, J. Microorganisms Pumping Iron: Anaerobic Microbial Iron Oxidation and Reduction. Nat. Rev. Microbiol. 2006, 4, (5) Pickering, I. J.; et al. Localizing the Biochemical Transformations of Arsenate in a Hyperaccumulating Fern. Environ. Sci. Technol. 2006, 40, (6) Brandes, J.; Ingall, E.; Paterson, D. Characterization of Minerals and Organic Phosphorus Species in Marine Sediments Using Soft X-ray Fluorescence Spectromicroscopy. Mar. Chem. 2007, 103, (7) Thornton, J. Pandora s Poison: Chlorine, Health, and a New Environmental Strategy; MIT Press: Cambridge, MA, (8) Nilsson, H. J.; et al. Soft X-ray Scanning Transmission X- ray Microscopy (STXM) of Actinide Particles. Anal. Bioanal. Chem. 2005, 383, (9) Chao, W.; et al. Soft X-ray Microscopy at a Spatial Resolution Better than 15 nm. Nature 2005, 435, (10) Quiney, H. M.; et al. Diffractive Imaging of Complex Highly Focused X-ray Fields. Nat. Phys. 2006, 2, (11) Thieme, J.; et al. X-ray Microscopy in the Energy Range <1 kev. In X-ray Spectromicroscopy and Environmental Sciences; Thieme, J., et al., Eds.; Topics in Applied Physics; Springer: New York, 2008, in press. (12) Thieme, J.; Schneider, G.; Knöchel, C. X-ray Tomography of a Microhabitat of Bacteria and Other Soil Colloids with Sub-100 nm Resolution. Micron 2003, 34, (13) Feser, M.; et al. Integrating Silicon Detector with Segmentation for Scanning Transmission X-ray Microscopy. Nucl. Instrum. Methods Phys. Res., Sect. A 2006, 565, (14) Thieme, J.; et al. Speciation of Sulfur in Oxic and Anoxic Soils Using X-ray Spectromicroscopy. In Proceedings of the 8th International Conference on X-ray Microscopy; Aoki, S., Kagoshima, Y., Suzuki, Y., Eds.; Institute of Pure and Applied Physics Conference Series 7, 2006; pp (15) Gleber, G.; et al. Interaction of Organic Substances with Iron Studied by O1s Spectroscopy Development of an Analysis Program. J. Phys. IV 2003, 104, (16) Lombi, E.; et al. Speciation and Distribution of Phosphorus in a Fertilized Soil: A Synchrotron-Based Investigation. Soil Sci. Soc. Am. J. 2006, 70, October 15, 2007 / Environmental Science & Technology n 6889
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