Influence of biogenic Fe(II) on the extent of microbial reduction of Fe(III) in clay minerals nontronite, illite, and chlorite
Introduction
Clay minerals are major components in soils, sedimentary rocks, and pelagic oozes blanketing the ocean basins (Moore and Reynolds, 1997). They play an important role in environmental processes such as nutrient cycling, plant growth, contaminant migration, organic matter maturation, and petroleum production (Stucki et al., 2002, Kim et al., 2004, Stucki, 2006). Iron is a major constituent in clay and clay minerals, and its mobility and stability in different environmental processes is, in part, controlled by the oxidation state (Stucki et al., 2002). Previous studies using chemical reductants such as sodium dithionite and hydrazine (Russell et al., 1979) have shown the effects of iron oxidation state on clay swelling, cation exchange and fixation capacity, specific surface area, color, and magnetic exchange interactions of clay minerals (Stucki et al., 2002, Stucki, 2006).
The structural ferric iron in clay minerals can be reduced either chemically or biologically (Gates et al., 1993, Gates et al., 1998, Kostka et al., 1996, Kostka et al., 1999a, Kostka et al., 1999b, Dong et al., 2003a, Dong et al., 2003b, Kim et al., 2004, Jaisi et al., 2005, O’Reilly et al., 2005, Stucki, 2006). These experiments have consistently shown that microbial reduction of Fe(III) often ceases before all Fe(III) in clay minerals is exhausted. The extent and rate of Fe(III) reduction determined in laboratory batch experiments may be underestimated relative to those in natural environments, due to the inhibition effect by sorption of biogenic Fe(II) onto cell and mineral surfaces in batch experiments (Roden and Urrutia, 1999, Roden and Wetzel, 2002, Roden and Urrutia, 2002). Quantification of this inhibition effect is important for model development and understanding of iron cycling in nature, where there may be natural mechanisms for removing or reducing the effect of Fe(II) sorption by dynamic flow, mineral precipitation, and complexation with organic and inorganic ligands (Roden and Zachara, 1996, Fredrickson et al., 1998, Roden and Urrutia, 1999, Urrutia et al., 1999, Roden et al., 2000, Roden and Urrutia, 2002, Royer et al., 2002, Royer et al., 2004). The extent of bioreduction may also be increased by addition of fresh cells to an old microbe-mineral culture, where bioreduction had stopped due to inactivation of iron-reducing bacteria by Fe(II) sorption (Urrutia et al., 1998).
Although the inhibitory effects of Fe(II) on the extent of microbial reduction of iron oxides have been relatively well documented in the literature (Hacherl et al., 2001, Roden and Urrutia, 2002), it is unclear whether Fe(II) will have similar inhibitory effects on microbial reduction of structural Fe(III) in clay minerals because clay minerals differ from iron oxides in mineral surface properties, Fe(III) structural locations, and Fe(II) sorption mechanisms. The cessation of microbial reduction of structural Fe(III) in clay minerals has often been reported (Kostka et al., 1999a, Kostka et al., 1999b, Dong et al., 2003a, Dong et al., 2003b), but experimental studies on the influence of biogenic Fe(II) on the bioreduction extent have not been performed. In this study, we investigated the inhibitory effects of Fe(II) on the extent of bioreduction of structural Fe(III) in clay minerals. Four different clay minerals were used in this study. The inhibitory effects of Fe(II) on cell activity and mineral reactivity were individually evaluated using the well-characterized redox mediator AQDS/AH2DS.
Section snippets
Clay mineral preparation
Four representative clay minerals were chosen in this study based on their differences in layer type, layer charge, interlayer swelling property, and crystal chemistry of Fe(III). Two nontronite (a iron-rich smectite, NAu-1, NAu-2) and chlorite (CCa-2) samples were purchased from the Source Clays Repository, IN. The two nontronites are different in terms of Fe(III) site occupancy (Gates et al., 2002) and the extent of bioreduction (Jaisi et al., 2005). Keeling et al. (2000) published the
Characterization of the clay minerals
The DCP measurement for total iron and titration measurement for ferrous iron showed that NAu-1 contained 16.4% iron by weight and 99.6% of that as Fe(III). Mössbauer spectroscopy and X-ray diffraction analyses revealed that NAu-1 also contained minor (∼12%) goethite and trace illite, quartz, and calcite (Table 1). NAu-2 consisted of pure nontronite, containing 23.4% iron by weight, 99.4% of that as Fe(III). Mu-Il contained 9.2% iron, 93% of which was Fe(III). This was a relatively pure illite
Inhibition of Fe(III) reduction by cell-sorbed Fe(II)
The progressively more severe inhibition effect on Fe(III) reduction resulting from an increasing amount of presorbed Fe(II) and the promotion effect as a result of removal of surface sorbed Fe(II) (in our two-step method) strongly suggests that cell-sorbed Fe(II) was an important factor responsible for controlling the extent of Fe(III) reduction. Our data suggest that this factor contributed to incomplete Fe(III) reduction in clay minerals. This type of cell-sorbed inhibition effect has been
Conclusion
Our results have collectively shown that Fe(II) sorption onto bacterial and clay mineral surfaces significantly inhibited reduction of Fe(III) in clay minerals. These Fe(II) inhibition effects at least partially contributed to cessation of Fe(III) bioreduction. When these effects were alleviated, the extent of Fe(III) was significantly enhanced. Using our new procedure (two-step method), the inhibition effects from cell- and clay-sorbed Fe(II) could be separately evaluated. This separation is
Acknowledgments
This research was supported by a grant from National Science Foundation (EAR-0345307) to H.D. Some part of this research was supported by student grants from the Clay Mineral Society (Student Research Grant, 2004) and AAPG (John Teagle Memorial Grant, 2004), Geological Society of America (Student Research Grant, 2005) to D.P.J. This research was also partially supported by US Department of Energy (DOE), Office of Science, through Environmental Remediation Science Program (ERSP). Pacific
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