Influence of biogenic Fe(II) on the extent of microbial reduction of Fe(III) in clay minerals nontronite, illite, and chlorite

https://doi.org/10.1016/j.gca.2006.11.027Get rights and content

Abstract

Microbial reduction of Fe(III) in clay minerals is an important process that affects properties of clay-rich materials and iron biogeochemical cycling in natural environments. Microbial reduction often ceases before all Fe(III) in clay minerals is exhausted. The factors causing the cessation are, however, not well understood. The objective of this study was to assess the role of biogenic Fe(II) in microbial reduction of Fe(III) in clay minerals nontronite, illite, and chlorite. Bioreduction experiments were performed in batch systems, where lactate was used as the sole electron donor, Fe(III) in clay minerals as the sole electron acceptor, and Shewanella putrefaciens CN32 as the mediator with and without an electron shuttle (AQDS). Our results showed that bioreduction activity ceased within two weeks with variable extents of bioreduction of structural Fe(III) in clay minerals. When fresh CN32 cells were added to old cultures (6 months), bioreduction resumed, and extents increased. Thus, cessation of Fe(III) bioreduction was not necessarily due to exhaustion of bioavailable Fe(III) in the mineral structure, but changes in cell physiology or solution chemistry, such as Fe(II) production during microbial reduction, may have inhibited the extent of bioreduction. To investigate the effect of Fe(II) inhibition on CN 32 reduction activity, a typical bioreduction process (consisting of lactate, clay, cells, and AQDS in a single tube) was separated into two steps: (1) AQDS was reduced by cells in the absence of clay; (2) Fe(III) in clays was reduced by biogenic AH2DS in the absence of cells. With this method, the extent of Fe(III) reduction increased by 45–233%, depending on the clay mineral involved. Transmission electron microscopy observation revealed a thick halo surrounding cell surfaces that most likely resulted from Fe(II) sorption/precipitation. Similarly, the inhibitory effect of Fe(II) sorbed onto clay surfaces was assessed by presorbing a certain amount of Fe(II) onto clay surfaces followed by AH2DS reduction of Fe(III). The reduction extent consistently decreased with an increasing amount of presorbed Fe(II). The relative reduction extent [i.e., the reduction extent normalized to that when the amount of presorbed Fe(II) was zero] was similar for all clay minerals studied and showed a systematic decrease with an increasing clay-presorbed Fe(II) concentration. These results suggest a similar inhibitory effect of clay-sorbed Fe(II) for different clay minerals. An equilibrium thermodynamic model was constructed with independently estimated parameters to evaluate whether the observed cessation of Fe(III) reduction by AH2DS was due to exhaustion of reaction free energy. Model-calculated reduction extents were, however, over 50% higher than experimentally measured, indicating that other factors, such as blockage of the electron transfer chain and mineralogy, restricted the reduction extent. Another important result of this study was the relative reducibility of Fe(III) in different clays: nontronite > chlorite > illite. This order was qualitatively consistent with the differences in the crystal structure and layer charge of these minerals.

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

References (55)

  • H. Dong

    Interstratified illite-smectite: a review of contributions of TEM data to crystal chemical relations and reaction mechanisms

    Clay Sci.

    (2005)
  • H. Dong et al.

    Microscopic evidence for microbial dissolution of smectite

    Clays Clay Miner.

    (2003)
  • H. Dong et al.

    Microbial reduction of structural Fe(III) in illite and goethite by a groundwater bacterium

    Environ. Sci. Technol.

    (2003)
  • V. Ernstsen et al.

    Microbial reduction of structural iron in clays—a renewable source of reduction capacity

    J. Environ. Quality

    (1998)
  • W.P. Gates et al.

    Swelling and texture of iron bearing smectites reduced by bacteria

    Clays Clay Miner.

    (1998)
  • W.P. Gates et al.

    Site occupancies by iron in nontronites

    Clays Clay Miner.

    (2002)
  • W.P. Gates et al.

    Swelling properties of microbially reduced ferruginous smectite

    Clays Clay Miner.

    (1993)
  • S.J. Gregg et al.

    Adsorption, Surface Area and Porosity

    (1982)
  • A. Grütter et al.

    Sorption desorptionand, isotope exchange of cesium on chlorite

    Clays Clay Miner.

    (1986)
  • E.L. Hacherl et al.

    Measurement of iron(III) bioavailability in pure iron oxide minerals and soils using anthraquinone-2,6-disulfonate oxidation

    Environ. Sci. Technol.

    (2001)
  • Harris, D., Schmitter, R., 2006. Global transcription regulation of iron-responsive genes in Shewanella oneidensis...
  • B-H. Jeon et al.

    Low-temperature oxygen trap for maintaining strict anoxic conditions

    J. Environ. Engg.

    (2004)
  • S. Katoh et al.

    Use of sodium polytungstate solution in the purification of volcanic glass shards for bulk chemical analysis

    Nat. Human Act.

    (1999)
  • J.L. Keeling et al.

    Geology and characterization of two hydrothermal nontronites from weathered metamorphic rocks at the Uley graphite mine, South Australia

    Clays Clay Miner.

    (2000)
  • J.W. Kim et al.

    Role of microbes in the smectite-to-illite reaction

    Science

    (2004)
  • J.E. Kostka et al.

    Respiration and dissolution of iron(III)-containing clay minerals by bacteria

    Environ. Sci. Technol.

    (1999)
  • J.E. Kostka et al.

    Reduction of structural Fe(III) in smectite by a pure culture of Shewanella putrefaciens strain MR-1

    Clays Clay Miner.

    (1996)
  • Cited by (0)

    View full text