Parameters Controlling the Partitioning of Trace Metals at the Shewanella oneidensis MR-1 Biofilm/Mineral/Water Interface: Long Period X-ray Standing Wave and XAFS Study

Microbial biofilms are common in natural and man-made environments and are often present as coatings on mineral surfaces in soils and aquatic systems. Compared to bare mineral surfaces, biofilms can induce significant changes in surface charges and sorption capacities for metal(loid) ions. However, the effects of biofilm coatings on mineral reactivity and metal cycling are still poorly understood at a molecular level due to the complex nature of these systems and the lack of appropriate tools to accurately probe such interfaces. In this study, we applied long-period X-ray standing wave-florescence yield (XSW-FY) spectroscopy to measure in-situ the partitioning of trace elements between S. oneidensis MR-1 biofilms and highly polished single crystal surfaces of alumina (1-102) and hematite (0001) as a function of several external parameters, including trace element concentration, pH, and time, we also studied competitive effects of different cations and anions by exposing the biofilm/mineral interface to different trace elements simultaneously. In addition, grazing incidence X- ray adsorption fine structure (GI-XAFS) spectroscopic measurements at specific x-ray incidence angles were conducted to probe ion speciation and local coordination environment at the mineral surface and in the biofilm. Long-period XSW-FY measurements on Pb(II) partitioning at S. oneidensis biofilm-coated alumina (1-102) and hematite (0001) surfaces under aerobic conditions indicate that Pb(II) is preferentially adsorbed on the mineral surface at low concentrations (10-7 to 10-6 M ) at pH 6.0 and is increasingly partitioned into the biofilm at higher concentrations (10-6 to 10-5 M). This finding indicates that S. oneidensis biofilm coatings do not block reactive sites on hematite and alumina. Decreasing solution pH from 6.0 to 4.0 for biofilm coated alumina (1-102) sample exposed to 10-6 M Pb(II) showed a shift of Pb(II) partitioning from interface to biofilm due to electrostatic effects. Significant changes in Pb(II) XSW-FY profiles at three different exposure times (30 minutes, 3 hours, and 1 day) on fresh samples in each case suggest that Pb(II) partitioning at the biofilm/mineral/water interface is diffusion limited. No apparent competitive effects were observed for Pb(II) and Zn(II). In addition, a variety of cations such as Ca(II), K, and Cu(II) were detected in biofilm-coated mineral samples, and each element exhibited a unique partitioning behavior. Results of Pb L3-edge GI-XAFS analysis of Pb(II)/S. oneidensis biofilm/hematite samples showed that carboxyl groups are responsible for Pb(II) complexation in the biofilm after 3 hours at pH 6.0. No evidence of biomineralization was observed under our experimental conditions. These studies provide new insights about the factors controlling trace element partitioning and speciation at complex microbe-mineral interfaces and an improved understanding of the nature of microenvironments created by microbial biofilms.