Trace Metal Retention
on Biogenic Manganese
Oxide Nanoparticles
Mario Villalobos1, John Bargar2, and Garrison Sposito3
M
Scanning electron
micrograph (Toner 2004;
Toner et al. 2005) of
Pseudomonas putida
MnB1 cells (cylinders)
and associated
manganese oxide particles
(curdy aggregates)
enmeshed in a biofilm.
Until recently, many important
aspects of the geochemistry of bacterial Mn oxides have remained
elusive, due largely to the poorly
crystalline, nanoparticulate, and
highly reactive nature of these
minerals. Investigations published
within the past few years, however,
have begun to shed light on the
molecular structures of bacterial
Mn4+ oxides and the mechanisms
that produce their well-known
KEYWORDS: biogenic manganese oxides, metal sorption reactions, strong affinities for trace metals.
trace metals, X-ray absorption spectroscopy We highlight these studies in this
paper, focusing on the extraordinary ability of Mn4+ oxides proINTRODUCTION
duced by the soil and freshwater bacterium Pseudomonas
Manganese oxides help govern the composition of natural putida strain MnB1 (FIG. 1) to retain the common and perwaters, the arability of soils, and the potability of both sub- nicious environmental trace metal contaminant, Pb2+.
surface and surface waters. These minerals are commonly
found in lakes and watersheds as suspended particles
(Davison 1993). In aquifers, soils, and river beds, where
their concentrations may exceed several weight percent
A
(Kabata-Pendias 2001), Mn oxides may occur as thin coatings on sediment grains (Post 1999; Fuller and Harvey
2000), thus masking the identity and suppressing the reactivity of the underlying mineral substrate. Owing to their
small particle size and malleable crystal structure, Mn
oxides are potent scavengers of trace metals in both terrestrial and aquatic environments, as documented in recent
reviews (Post 1999; Nelson and Lion 2003; O’Reilly and
Hochella 2003; Tebo et al. 2004).
anganese oxides produced by microorganisms are abundant environmental nanoparticles whose high retention capacity for toxic trace
metals, especially lead, is well established. Until very recently, our
knowledge of the molecular-scale structure and reactivity of these biogenic
Mn4+ oxide minerals was inferred from studies of synthetic analogues prepared in the laboratory. However, biogenic Mn oxides and their reactions
with trace metals now can be investigated directly using X-ray absorption
spectroscopy, thus bringing new insights into the molecular mechanisms
behind the very high scavenging efficiency of these minerals. This new
knowledge has important implications for the remediation of trace
metal contamination.
Mn4+ oxides are formed by the oxidation of soluble and, in
subsurface environments, relatively mobile Mn2+, which
occurs typically in soils and groundwaters at concentrations
between 0.001 and 1 millimolar (Kabata-Pendias 2001).
Oxidation of soluble Mn2+ is thermodynamically favored,
but is generally very slow in natural waters (Morgan 2000,
2005). Bacteria and fungi, however, have been shown, both
in the laboratory and in a broad variety of field settings, to
accelerate the oxidation of Mn2+ by several orders of magnitude (Tebo et al. 1997; Morgan 2000; Nelson and Lion
2003; Tebo et al. 2004; Morgan 2005). These findings have
led to the current postulate that Mn4+ oxides found in the
environment are largely of biological origin (i.e. biogenic).
B
1 Environmental Bio-Geochemistry Group, LAFQA
Instituto de Geografía, Universidad Nacional Autónoma de México
(UNAM), Coyoacán, 04510, D.F., México
E-mail: [email protected]
2 Stanford Linear Accelerator Center
2575 Sand Hill Road, MS 69, Menlo Park, CA 94025, USA
3 Environmental Geochemistry Group, Division of Ecosystem Sciences
University of California, Berkeley, CA 94720-3114, USA
ELEMENTS, VOL. 1,
PP.
223–226
Transmission electron micrographs (Toner 2004; Toner et
al. 2005) showing a P. putida cell with its associated Mn
oxide (A) and a section view of the Mn oxide nanoparticles (B).
223
FIGURE 1
S EPTEMBER 2005
by negatively charged sites in the oxides
and by inner-sphere surface complexation
of the metals (i.e. direct chemical binding
of the metals to the mineral surface; see
Sparks in this issue). Nearly all of this
research, however, has involved synthetic
Mn oxides. The most detailed studies
have been done on well-crystallized minerals, which may differ substantially in
structure and reactivity from the poorly
crystalline varieties expected as products
of microbially mediated Mn2+ oxidation
(Tebo et al. 2004).
Common birnessite minerals. Natural birnessites become
less crystalline as the concentration of Mn3+ in their structures decreases. Triclinic birnessite (left) contains the maximum amount
of Mn3+ substitution—about one-fourth of the octahedra—and has no
cation vacancies, whereas d-MnO2 (right) exhibits no Mn3+ substitution
but has several mol percent cation vacancies. Pb2+ sorption complexes
are illustrated for d-MnO2. Well-crystallized hexagonal birnessite has
about 10% Mn3+ substitution and about 16% cation vacancies that bind
interlayer Mn2+ and Mn3+. The birnessite mineral produced by P. putida
MnB1 has hexagonal symmetry and, although it has the same proportion of vacancies as hexagonal birnessite, it shows no Mn3+ substitution
and thus has a lower crystallinity than the latter mineral. As crystallinity
decreases, birnessite minerals develop high external specific surface
areas characteristic of nanoparticles. Recently, it has been possible to
prepare synthetic birnessites without Mn3+, but with high crystallinity,
by employing very-high-temperature conditions (Gaillot et al. 2003).
However, natural samples and those synthesized at lower temperatures
seem to follow the trend described above.
FIGURE 2
These new results have important implications for the
retention of trace metals in natural settings and for the
bioremediation of metal-contaminated environments.
Laboratory research directed toward understanding the
molecular biology of Mn2+ oxidation by bacteria has
focused on three model organisms, all of which oxidize
Mn2+ in a polymer matrix outside the cell (Tebo et al. 1997,
2004; Brouwers et al. 2000): (1) Bacillus sp. strain SG-1, a
marine bacterium that produces Mn2+-oxidizing spores; (2)
Leptothrix discophora, a freshwater bacterial species that
deposits Mn4+ oxides on its extracellular sheath; and (3)
Pseudomonas putida strain MnB1, a common freshwater and
soil bacterium that precipitates Mn4+ oxides on the cell surface (FIG. 1). Pseudomonas putida forms a biofilm comprising
extracellular polymers that enmesh both the bacterial cells
and the Mn oxides they produce. However, the organic
sorption sites in biofilms do not appear to compete effectively with Mn4+ oxides in scavenging trace metals, if the
metal concentration is low (Nelson et al. 1999b; Dong et al.
2000; Wilson et al. 2001; Toner 2004).
TRACE METAL RETENTION
ON BIOGENIC Mn4+ OXIDES
Nelson and Lion (2003), O’Reilly and Hochella (2003), and
Tebo et al. (2004) have reviewed laboratory research on the
mechanisms of trace metal retention on synthetic and biogenic Mn4+ oxides. They noted the important role played
ELEMENTS
The mineral name “birnessite” is generally
used to designate Mn4+ oxides with a
layer structure comprising mainly
Mn4+O6 octahedra that share edges to
form extensive sheets (Dixon and White
2002). Following Villalobos et al. (2003),
we shall use this name to include all such
Mn oxide minerals that have a layer structure and either triclinic or hexagonal symmetry, including “d-MnO2” and “vernadite,” minerals whose names in the past
often have been distinguished from “birnessite.” The sheets making up a birnessite crystal may be stacked with differing degrees of order,
including completely random stacking (i.e. no threedimensional order). The hexagonal varieties contain mostly
Mn4+ in the layers, whereas the triclinic varieties (Lanson et
al. 2002; Manceau et al. 2002) exhibit a significant proportion of Mn3+ substitutions (FIG. 2). Synthetic samples of this
latter variety show high crystallinity. Natural samples,
which are mostly hexagonal, are invariably reported as
being poorly crystalline and sprinkled with Mn4+ vacancies
without structural Mn3+ (Lanson et al. 2004; Villalobos et
al. in press).
The Mn oxide produced by P. putida MnB1 is a poorly crystalline birnessite with hexagonal symmetry (Villalobos et
al. 2003; Villalobos et al. in press), which contains only
edge-sharing Mn4+O6 octahedra in its layers, with one-sixth
of the cation (Mn4+) sites vacant. This latter defect results in
negative charge on the structure, which is balanced by
Mn2+ and Mn3+, along with other solvated metal cations or
protons, in the interlayer region. The Mn oxide crystallites
produced by P. putida MnB1 each contain an average of
only three stacked sheets and extend for roughly 8–9 nm in
the horizontal plane, making them truly nanoparticles that
are highly reactive with trace metals and environmental
chemicals (Lanson et al. 2004; Bargar et al. 2005; Villalobos
et al. in press).
Jürgensen et al. (2004) investigated the structure of the
Mn4+ oxide produced by L. discophora SP-6 and found that
the crystallites of this biogenic mineral are composed of single birnessite layers. Their result calls into question a proposal by Kim et al. (2003) that this Mn4+ oxide resembles
todorokite, which comprises triple chains of Mn4+O6 octahedra arranged to form a tunnel structure (Post 1999).
MECHANISMS OF Pb2+ RETENTION
ON SYNTHETIC BIRNESSITE
Tebo et al. (2004) highlighted the unusually strong retention of Pb often exhibited by natural Mn oxides in terrestrial and aquatic environments. For example, in biofilms
sampled from freshwater lakes, Nelson et al. (1999b) and
Dong et al. (2000, 2003) inferred highly preferential retention of Pb on Mn oxides relative to Fe oxides. High sorption
affinity of Mn oxides in natural soils and sediments for
224
S EPTEMBER 2005
other bivalent trace metal cations, such as Cd, Co, Ni, and
Zn, also has been reported (Tebo et al. 2004; Manceau et al.
2003). Nelson et al. (1999a, 2002) and Tani et al. (2004)
demonstrated a much greater retention of divalent trace
metals on biogenic Mn oxides than on their synthetic analogue. Nelson et al. (1999a, 2002) determined the remarkably high Pb retention capacity of 0.55 mol Pb per mol Mn
on the Mn oxide produced by L. discophora SS-1; this
biogenic Mn oxide had an affinity for Pb ten times greater
than that displayed by d-MnO2, a synthetic birnessite
(FIG. 2). Nelson et al. (2002) and Tani et al. (2004) thus proposed that biogenic Mn oxides could be used to remove
toxic metals from wastewaters.
Matocha et al. (2001) observed fast, irreversible kinetics for
retention (or sorption) of Pb2+ on synthetic “acid birnessite,”
along with the endothermic high-affinity reaction and lack
of ionic strength dependence that point to a tenacious sorption mechanism (Sposito 2004). Extended X-ray absorption
fine-structure (EXAFS) analyses of Pb sorption on “acid birnessite” and synthetic hexagonal birnessite led Matocha et
al. (2001) and Manceau et al. (2002), respectively, to propose
that Pb2+ was retained as an inner-sphere surface complex
on octahedral vacancy sites, with the Pb ion in a distorted
trigonal pyramid coordination (FIG. 2). This configuration
was first proposed by Bargar et al. (1997) and is a reasonable
hypothesis, since in “acid birnessite” about one-eighth of
the Mn4+ octahedral sites are vacant (Lanson et al. 2004;
Villalobos et al. in press), while in hexagonal birnessite
about one-sixth of the Mn4+ sites are vacant with another
one-twelfth occupied by Mn3+. The EXAFS analyses also
ruled out a redox-based retention mechanism (i.e. no spectral evidence for oxidation of Pb2+ to Pb4+) or surface cluster formation. Thus the mechanism of Pb retention on birnessite was interpreted as one of rapid uptake into the
interlayer region followed by migration of Pb to an octahedral vacancy, which, in the absence of protonation, exposes
three reactive oxygen sites (FIG. 2).
Villalobos et al. (2005) noted that the published retention
capacities for Pb on synthetic and biogenic Mn oxides varied
widely, despite being measured under similar experimental
conditions. They suggested that the large variation in Pb
retention capacity can be explained in terms of a simple
model based on two types of Pb, one residing in the interlayer region of a crystallite (Pbint) and one residing on its
external surfaces (Pbext):
mol Pb sorbed = mol Pbint + mol Pbext
Dividing both sides of this equation by the number of
moles of Mn in the sample, one deduces a model equation
for total maximum mol Pb sorbed per mol Mn (Pb/Mn):
Pb/Mn = xPbint + µr Gext Sa
where xPbint is the contribution to Pb/Mn from sorption in
the interlayer, µr is the relative molecular mass of the Mn
oxide in the sample, Gext is the average number of moles of
Pb sorbed per unit area of external surface, and Sa (m2 g-1) is
the external specific surface area of the Mn oxide. This
model equation predicts that, at a given pH (since protons
will compete with Pb2+ for sorption sites), the maximum
Pb/Mn will be a linear function of Sa. Villalobos et al. (2005)
compiled data on maximum Pb sorption at pH = 6 by five
birnessites, both synthetic and biogenic, whose external
specific surface area was known. They then performed linear regression analysis to find the relationship:
Pb/Mn = 0.0891 + 0.0020 Sa
ELEMENTS
(r2 = 0.993**)
with Sa ranging from 41 to 224 m2 g-1. Two mechanisms of
Pb sorption are thus indicated, but evidently Mn oxide crystallites are small enough in most cases that external edge
surfaces play a more important role than do interlayers.
Villalobos et al. (2005) performed an extensive EXAFS
analysis of Pb sorbed on three birnessites, one biogenic, the
other two being d-MnO2 and “acid birnessite” (FIG. 2). The
EXAFS spectra could be simulated precisely by considering
a total of four different “shells” of neighboring atoms
around Pb2+ for all oxides and sorption conditions investigated: an inner shell of oxygens at ca 0.231 nm and three
more distant shells of Mn atoms at ca 0.353, 0.371, and
0.550 nm. Pb2+ coordination complexes that display a
0.23 nm Pb–O bond length typically involve a highly distorted, trigonal pyramid first-shell coordination geometry
(FIG. 2), with three oxygens (or hydroxyls) forming the triangular base and the Pb lone-pair electrons defining the
pyramid apex (Bargar et al. 1997).
Accurate simulation of the EXAFS spectra in fact required
two different sorption complexes: one typical of the expected
interlayer species (comprising 25–50% of total Pb2+) and
another consistent with a surface complex at particle edges
(50–75% of Pb2+) (FIG. 2). Thus, the EXAFS simulations were
consistent with significant Pb retention on external particle
edge surfaces, supporting the empirical correlation found
between Pb/Mn and external specific surface area. The
0.550 nm third-shell (Pb–Mn) distance determined by the
EXAFS analysis corresponds to a second shell of Mn atoms
for the interlayer complex (FIG. 2).
The reactivity of interlayer and crystallite edge sites with
cations should be high, because each O2- at these sites is
only singly coordinated to a Mn4+ center instead of being
triply coordinated as in the bulk structure. Sorption of Pb2+
at both types of sites thus stabilizes undercoordinated O2-,
especially if Pb is also coordinated to a hydroxide ion and
water molecules. Both of the Pb species illustrated in FIG. 2
can react with three protons, which displace them and produce stable protonated surface species (Villalobos et al.
2005). This exchange is consistent with the observed competition between Pb2+ and protons for sorption sites on birnessite (Matocha et al. 2001; Villalobos et al. 2005).
Biogenic Mn oxides thus have two strong metal cation retention mechanisms: the structural binding of species at interlayer sites and the binding of species at the external edges
of crystallites. These mechanisms explain the observed high
affinity of birnessite nanoparticles for Pb. The availability of
very large specific surface areas (small particle size) and
high-affinity binding sites with differing stereochemical
properties implies that biogenic Mn oxides are strong sorbents for a variety of toxic metal cations. This conclusion
provides a scientific basis for their proposed use in the
designed remediation of metal-contaminated wastewaters,
soils, and sediments (Nelson et al. 2002; Tani et al. 2004).
ACKNOWLEDGMENTS
We thank Sam Webb (Stanford Synchrotron Radiation
Laboratory) for technical assistance with EXAFS analysis.
Brandy Toner and Gordon Vrdoljak (University of
California at Berkeley) are thanked for the electron micrographs. This research was partially supported by the NSF
Collaborative Research Activities in Environmental
Molecular Science program, grant CHE-0089208. Stanford
Synchrotron Radiation Laboratory is a national user facility
operated on behalf of the US Department of Energy, Office
of Basic Energy Sciences. .
225
S EPTEMBER 2005
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