Biogeochemical Properties of Bacteriogenic Iron Oxides

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(bacteriogenic iron oxides) to acknowledge that chemical and/or bacterial oxidation of Fe2+ produces Fe3+, which may then pre- cipitate on bacterial cells ...
Geomicrobiology Journal, 22:79–85, 2005 c Taylor & Francis Inc. Copyright  ISSN: 0149-0451 print / 1362-3087 online DOI: 10.1080/01490450590945861

Biogeochemical Properties of Bacteriogenic Iron Oxides F. G. Ferris Department of Geology, University of Toronto, Toronto, Ontario M5S 3B1, Canada

solid phase reactivity of each individual cell. Among the myriad of geochemical processes in which bacteria participate, redox and phase (i.e., dissolved versus solid) transformations of Fe are extremely sensitive to bacterial manipulation. This is because under appropriate redox conditions, Fe2+ serves as an electron donor for lithotrophic bacterial growth (Emerson and Revsbech 1994; Emerson and Moyer 1997; Edwards et al. 2003, 2004; Emerson and Weiss 2004), whereas Fe3+ compounds can act as electron acceptors for anaerobic respiration (Lovley 1997; Lovley and Coates 2000). A distinguishing feature of the Fe2+ /Fe3+ redox couple is that Fe3+ is prone to hydrolysis and precipitation (Schwertmann et al. 1995; Majlan et al. 2004). Metals that undergo hydrolysis in solution also tend to sorb strongly and specifically to surfaces of reactive solids, including bacterial cells (Stumm and Morgan 1996; Warren and Ferris 1998). Fe3+ in particular is bound tenaciously by bacteria and commonly precipitates to form hydrous ferric oxide (HFO) coatings on cell surfaces (Ferris et al. 1989; Fortin et al. 1993; Kennedy et al. 2003). These HFO precipitates are themselves highly reactive (Dzombak and Morel 1990) and comprise an additional sorbent phase for dissolved metals on the bacteria. Because of their broad distribution and reactive surface properties, HFO are considered to be dominant sorbents of dissolved metals in aquatic environments (Stumm and Morgan 1996); however, this idea is not written in stone as a considerable body of work exists which shows that natural Fe oxides frequently contain significant amounts of organic matter, particularly intact and partly degraded bacterial cells (Ferris et al. 1989, 1999; Filella et al. 1993; Fortin et al. 1993; Kennedy et al. 2003). These mixtures of HFO and bacteria have inherited the acronym BIOS (bacteriogenic iron oxides) to acknowledge that chemical and/or bacterial oxidation of Fe2+ produces Fe3+ , which may then precipitate on bacterial cells (Hallbeck and Pedersen 1990, 1991; Warren and Ferris 1998; Anderson and Pedersen 2003). The intent of this short review is to consider in turn how BIOS form in natural environments, interact with dissolved metals, and are characterized by unique surface chemical properties. An emphasis throughout the discussion is the occurrence of BIOS in circumneutral pH systems, on which many recent investigations have focused (Kennedy et al. 2003; Edwards et al. 2003, 2004; Emerson and Weiss 2004; Sobolev and Roden 2004).

Bacteriogenic iron oxides (BIOS) are composite materials that consist of intact and partly degraded remains of bacterial cells intermixed with variable amounts of poorly ordered hydrous ferric oxide (HFO) minerals. They form in response to chemical or bacterial oxidation of Fe2+ , which gives rise to Fe3+ . Once formed, Fe3+ tends to undergo hydrolysis to precipitate in association with bacterial cells. In acidic systems where the chemical oxidation of Fe2+ is slow, bacteria are capable of accelerating the reaction by several orders of magnitude. At circumneutral pH, the chemical oxidation of Fe2+ is fast. This requires Fe2+ oxidizing bacteria to exploit steep redox gradients where low pO2 slows the abiotic reaction enough to allow the bacteria to compete kinetically. Because of their reactive surface properties, BIOS behave as potent sorbents of dissolved metal ions. Strong enrichments of Al, Cu, Cr, Mn, Sr, and Zn in the solid versus aqueous phase (log 10 Kd values range from 1.9 to 4.2) are common; however, the metal sorption properties of BIOS are not additive owing to surface chemical interactions between the constituent HFO and bacteria. These interactions have been investigated using acid-base tritrations, which show that the concentration of high pKa sites is reduced in BIOS compared to HFO. At the same time, hydroxylamine insoluble material (i.e., residual bacterial fraction) is enriched in low pKa sites relative to both BIOS and HFO. These differences indicate that low pKa or acidic sites associated with bacteria in BIOS interact specifically with high pKa or basic sites on intermixed HFO. Keywords

bacteria, bacteriogenic, ferric, ferrous, iron, geochemistry, oxidation, oxide

INTRODUCTION Bacteria are recognized increasingly as major protagonists in a wide range of geochemical reactions in both pristine and contaminated aqueous environments. The behavior of bacteria as chemically reactive “agents provocateurs” is engendered not only by a ubiquitous ecological distribution and diverse spectrum of metabolic capabilities, but also stems from the intrinsic

Received 15 November 2004; accepted 22 February 2005. The author’s work is supported by the Natural Sciences and Engineering Research Council (NSERC) of Canada. Address correspondence to F. G. Ferris, Department of Geology, University of Toronto, 22 Russell Street, Toronto, Ontario M5S 3B1, Canada. E-mail: [email protected]

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F. G. FERRIS

Fe3+ + nH2 O ↔ Fe(OH)(3−n)+ + nH+ n

[1]

As pH (i.e., the concentration of protons decreases) or the total concentration of Fe3+ in solution increases, the relative proportion of hydrolyzed species in solution increases. Once the Fe3+ to proton ion activity product (IAP) exceeds that of a corresponding solid mineral phase at equilibrium (i.e., the solubility product K so ), for example ferrihydrite (considered in terms of equation 1 as FeOH3 ), solutions become oversaturated and precipitation may occur depending on whether the point of critical oversaturation has been reached (Warren and Ferris 1998; Majzlan et al. 2004). In thermodynamic terms, this is when the bulk free energy determined by saturation state is greater than the interfacial free energy arising from the formation of a new solid in the system (Stumm and Morgan 1996). The precipitation of ferric iron in association with bacterial cell surface polymers is an energetically favored process that evolves through a continuum of reactions (Warren and Ferris 1998). At first, sorption reactions dominate as reactive cell surface sites (e.g., carboxyl and phosphoryl groups) complex dissolved Fe3+ arising from chemical or microbial oxidation of Fe2+ . Once these surface sites become saturated, dissolved Fe3+ concentrations will increase until the point of critical oversaturation is reached (Figure 1). Because all bacterial cell surfaces are capable of interacting chemically with hydrous ferric oxides, the interfacial free energy that retards formation of stable HFO nuclei is reduced (Warren and Ferris 1998; Smith and Ferris 2003). This, in turn, decreases the point of critical oversaturation at which nucleation occurs in the absence of bacteria, and promotes precipitation directly on the surfaces of bacterial cells to form BIOS composites (Ferris et al. 1999, 2000; Fortin and Chatellier 2003). Recent studies documenting the behavior of bacterial cells as heterogeneous nucleation templates

-1

HFO Kso

-2 log ([Fe3+]solid )

Formation and Composition BIOS comprise a distinct family of composite materials that consist of intact and partially degraded remains of bacterial cells intermixed with variable amounts of poorly ordered hydrous ferric oxides (Ferris et al. 1999, 2000; Anderson and Pedersen 2003). Considerable variation exists in BIOS mineralogy and microbiology depending on the aqueous geochemistry of the environment in which they form (Bigham et al. 1996; Kasama and Murakami 2001); however, it is possible to distinguish two general categories of BIOS based on the influence of pH on both solid phase mineral speciation and microbial habitat. Recognition of the concept of pH as a master variable cannot be overemphasized because proton condition is such an important factor in regulating the rate and extent of biogeochemical reactions that contribute to BIOS formation. These reactions include chemical and microbial oxidation of soluble Fe2+ , as well hydrolysis and precipitation of Fe3+ (Stumm and Morgan 1996). In solution, dissolved Fe3+ tends to undergo hydrolysis with water to liberate protons:

-3

Precipitation -4 -5

Critical Oversaturation

-6

Sorption -7 0

2

4 3+

6

8

+ 3

log ([Fe ]dissolved/[H ] ) FIG. 1. Sorption and precipitation of Fe3+ in the presence of Bacillus subtilis (after Warren and Ferris 1998).

for HFO have applied advanced spectroscopic techniques (e.g., X-ray photoelectron emission spectromicroscopy and X-ray absorption near edge structure spectroscopy) to show that some bacteria extrude polysaccharide fibers to localize HFO precipitation at the cell surface, presumably to harness proton gradients for energy production (Chan et al. 2004). Under acid sulfate conditions, for example in mine drainage environments and some hot springs, the chemical oxidation of Fe2+ is very slow (Stumm and Morgan 1996). Conversely, at circumneutral pH values that characterize most surface water systems, the chemical oxidation of Fe2+ is fast (Neubauer et al. 2002). This difference in kinetics of Fe2+ oxidation gives rise to two distinct ecophysiological strategies among lithotrophic bacteria that exploit the Fe2+ /Fe3+ redox couple to generate energy for growth. Those that live in low pH habitats, such as Acidithiobacillus ferroxidans, are capable of oxidizing Fe2+ up to 1000 times faster than the chemical oxidation rate (Kasama and Murakami 2001). On the other hand, the fast chemical oxidation of Fe2+ at circumneutral pH requires lithotrophs like Gallionella ferruginea or Leptothrix ochracae to subsist under low pO2 microaerobic conditions, which slows Fe2+ oxidation to a point where the bacteria are able to compete kinetically with the abiotic reaction (Neubauer et al. 2002; James and Ferris 2004). The importance of low pO2 environments for circumneutral pH Fe2+ -oxidizing bacteria is illustrated in a study on a groundwater spring in northern Ontario, Canada (James and Ferris 2004). At the study site the greatest volume of flocculent BIOS precipitate was observed right at the spring source, and decreased significantly in amount downstream from the spring. Within the first 3.5 meters downstream of the spring, a sharp redox gradient existed that ranged from microaerobic Fe2+ -rich groundwater at the discharge point to a well aerated stream depleted in both reduced and oxidized species of dissolved iron (Figure 2). This gradient evolved evidently from rapid bacterial oxidation of dissolved Fe2+ followed by chemical hydrolysis and precipitation of Fe3+ . Scanning electron microscope examination of BIOS from the spring revealed both L. ochracea and G.

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TABLE 1 Ferrous iron oxidation rate constants, half reaction times, and initial reaction rates in spring groundwater microcosms both in the absence and presence BIOS (James and Ferris 2004)

3.0

0.21

2.5 0.20

0.19

1.5 1.0

0.18

Fe(II) (mg/L)

Eh (V)

2.0

0.5 0.17

Microcosm Chemical control Na-azide control BIOS

Rate constant k (min−1 )

t1/2 (min)

Oxidation rate (mmol L−1 min−1 )

0.024 0.056 0.147

28.9 12.4 4.7

0.0017 0.0022 0.0086

0.0 0.16 -2

0

2

4

6

8

-0.5 10

Distance from source (m)

FIG. 2. Redox potential (Eh) and dissolved ferrous iron (Fe2+ ) in 0.22 µm filtered water as a function of distance from a groundwater spring in northern Ontario, Canada (after James and Ferris 2005).

ferruginea (Figure 3). Of the two bacteria, L. ochracea sheaths comprised the greatest proportion of the BIOS, while helical G. ferruginea stalks were less abundant. The dominance of L. ochracea over G. ferruginea has been reported in a number of studies on circumneutral pH Fe2+ oxidizing bacteria (Emerson and Revsbech 1994; Kennedy et al. 2003). Although the reason for this is not known, L. ochracea

FIG. 3. Scanning electron micrograph of BIOS from a groundwater spring in northern Ontario, Canada, showing sheaths of Leptothrix ochracae (L) and a helical stalk from Gallionella ferruginea (G). Scale bar = 1.0 µm.

seems to thrive in situations where no other major electron donors (i.e., energy yielding substrates) are available apart from Fe2+ (Emerson and Revsbech 1994; Søgaard et al. 2001). Among other Fe2+ -oxidizing bacteria that have been isolated, notably those within the β-proteobacteria group like G. ferruginea, luxuriant mixotrophic and even organotrophic growth has been demonstrated (Hallbeck and Pedersen 1991; Siering and Ghiorse, 1996; Sobelev and Roden 2004). Based on these observations, it has been hypothesized that L. ochracea (which has not yet been isolated in pure culture) not only grows principally as a lithoautoroph, but is additionally capable of out competing other Fe2+ oxidizing bacteria for dissolved Fe2+ under nutrient conditions otherwise restrictive to mixotrophy and organotrophy. Microcosm experiments were also conducted in the groundwater spring study to assess whether bacteria enhance Fe2+ oxidation in reduced groundwater at circumneutral pH (James and Ferris 2004). The reaction rate constant for untreated BIOS was found to be nearly 3 times greater than that obtained with sodium azide-treated (i.e., killed) BIOS, and 6 times greater than the chemical oxidation (i.e., sterile control) rate constant (Table 1). The difference in rate constants between the sterile chemical control and sodium azide treatment relates to catalysis of Fe2+ oxidation by surfaces of iron oxides and dead bacteria (Neubauer et al. 2002; Jeon et al. 2003). Bacterial metabolic oxidation of Fe2+ is, in turn, evident from the rate constant increase between sodium azide-treated and living BIOS, which corresponds to approximately 61% of the total Fe2+ oxidation budget. This proportion agrees extremely well with other reports that indicate bacteria account for least 50% and up to 90% of Fe2+ oxidation at circumneutral pH, particularly under diffusion limiting conditions at aerobic-anaerobic interfaces (Emerson and Revsbech 1994; Neubauer et al. 2002; Sobolev and Roden 2004). In circumneutral pH environments, BIOS mineralogy is usually dominated by 2-line ferrihydrite, nominally 5Fe2 O3 ·9H2 O (Jambor and Dutrizac 1998; Kasama and Murakami 2001; Kennedy et al. 2003). This poorly ordered hydrous Fe oxide acts as a highly reactive sorbent of dissolved mineral-forming elements (Dzombak and Morel 1990), and such behavior is enhanced when ferrihydrite precipitates in association with bacteria to form intermixed BIOS composites (Ferris et al. 2000; Anderson and Pedersen 2003). The crystal structure of 2-line

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ferrihydrite is not well defined because of the absence of well defined peaks in XRD patterns (Jambor and Dutrizac 1998). In EXAFS studies, the Fe-(O, OH) bond lengths in ferrihydrite are consistent with octrahedral coordination of Fe3+ , as in goethite (Jambor and Dutrizac 1998). Other investigations suggest that up to 25% of the Fe3+ in ferrihydrite enjoys tetrahedral coordination at the surface of the mineral, while the bulk phase is similar to that of octahedral oxyhydroxides (Jambor and Dutrizac 1998). By way of contrast, a wide variety of mineral precipitates are associated with BIOS in acidic systems including ferrihydrite, goethite (α-FeOOH), jarosite [(H, Na, K)Fe3 (OH)6 (SO4 )2 ], and schwertmannite (Fe8 O8 (OH)6 SO4 ) (Schwertmann et al. 1995; Bigham et al. 1996). Among these, schwertmannite is formed generally in the pH range of 3.0 to 4.5, whereas jarosite tends to become significant at pH values below 3.0. Dissolved Metal-BIOS Interactions The structural polymers in cell walls and external sheaths of bacteria, including those that sorb Fe3+ , contain abundant acidic functional groups (i.e., carboxyl, phorphoryl, phosphodiester, amino) (Cox et al. 1999; Sokolov et al. 2001). Similarly, hydrous Fe oxide surfaces are characterized by the presence of amphoteric functional groups (Dzombak and Morel 1990): + − + S − OH+ 2 ↔ S − OH + H ↔ S − O + 2H

Proton exchange reactions involving these kinds of functional groups not only impact surface charge development, and but also mediate chemical interactions with dissolved ions and suspended solids. Consequently, BIOS composites exhibit a high degree of surface chemical heterogeneity and reactivity (Martinez et al. 2003). A considerable amount of work has been done on the metal ¨ o Hard Rock retention properties of BIOS at the 460 m deep Asp¨ Laboratory (HRL) near Oskarshamn on the east coast of Sweden. These studies include chemical “disection” of the composites using hydroxylamine extractions to obtain soluble oxide and insoluble bacterial fractions, as well as investigations on the influence of compositional variation in metal content of intact BIOS (Ferris et al. 1999; Anderson and Pedersen 2003; Martinez et al. 2003). At the HRL, BIOS precipitates develop commonly at locations where neutral to slightly alkaline (pH 7.0 to 8.0) groundwater flows out of hydraulically conductive fractures (Laaksoharju and Sk˚arman 1995). The BIOS precipitates form at such discharge points principally in response to extensive oxidation of Fe2+ and growth of G. ferruginea (Pedersen and Karlson 1995). The solid-phase partition coefficients (Kd values, presented in ¨ o BIOS reveal up to 3 or 4 orders of Table 2 as log Kd) for the Asp¨ magnitude enrichment over corresponding dissolved metal concentrations, notably for Mn, Cr, Cu, Zn, and Al. Among these metals, Cr (60%) and Mn (99%) were associated mainly with the oxide fraction, whereas Cu (79%), Zn (78%), and Al (70%)

TABLE 2 ¨ o BIOS, Dissolved and solid phase metal concentrations in Asp¨ oxide (hydroxylamine soluble), and bacterial cell (hydroxylamine insoluble) fractions (Martinez et al. 2003) Concentration (ppm)a Metal Al Ca Cr Cu K Mg Mn Na Sr Zn

Aqueous phaseb BIOS 0.975 869 0.003 0.032 20.2 113 1.42 1600 15 0.047

Oxide (%)c

Bacterial (%)c

6708 2048 (30.5) 4659 (69.5) 29170 26795 (92.0) 2374 (8.0) 42.6 25.4 (59.8) 17.1 (40.2) 67.3 14.3 (21.3) 53.0 (78.7) 4797 1058 (22.1) 3738 (77.9) 5573 820 (14.7) 4752 (85.3) 15745 15722 (99.8) 22.5 (0.2) 2796 1087 (38.9) 1708 (61.1) 1153 915 (79.4) 237 (20.6) 141 31.2 (22.1) 109 (77.9)

Log Kdd BIOS 3.8 1.5 4.2 3.3 2.4 1.7 4.0 0.2 1.9 3.5

Relative standard deviations are ≤10% of reported mean values. Aqueous phase refers to the filtrate after removal of solid phase BIOS by filtration. c Percentage of corresponding metal concentration in the BIOS composite. d Kd is solid phase metal concentration in the BIOS divided by the corresponding dissolved concentration in the aqueous phase. a

b

displayed a higher affinity for the bacterial fraction. Cu and Zn in particular have been shown to be strongly associated with organic matter in solid particulates (Warren and Zimmerman 1994). These observations are consistent with variations in BIOS Kd as a function of Fe oxide content, which indicate that the increasing amounts of bacterial organic matter contributes to enhanced solid-phase metal partitioning (Ferris et al. 1999, 2000; Anderson and Pedersen 2003). The principle of additivity in composite sorbent materials is an important consideration for development of a full understanding of metal ion interactions with BIOS (Vermeer et al. 1999; Small et al. 2001). Stated simply, the reactivity of a composite solid would be considered additive if the sum of metal sorption by the end-member components equals that of the intact composite (Vermeer et al. 1999). Should the amount of metal sorbed by a composite solid differ from the summed amount sorbed by the individual end-members, then this would constitute a deviation from additivity, which implies that specific surface chemical interactions exist between end-member solid phase functional groups (Vermeer et al. 1999; Smith and Ferris 2003). In a study measuring Sr2+ sorption by synthetic BIOS comprised of Shewanella alga and 2-line ferrihydrite (Small et al. 2001), the composite exhibited a maximum binding capacity for Sr2+ of 0.034 mmol/g, or 21% less than the amount calculated to be sorbed (0.043 mmol/g) based on the sorptive characteristics of each solid (i.e., S. alga and 2-line ferrihydrite) and their mass

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Interrogation of Specific Surface Chemical Interactions Acid-base titrations are an excellent way to probe the surface reactivity of natural sorbent solids. There are a number of ways to fit experimental titration data, including but not limited to linear programming and regularized least-squares (Smith and Ferris 2001). In addition, methods are available to obtain distribution functions of acid dissociation constants (i.e., Ka values) directly from experimental data using derivative techniques combined with smoothing algorithms. The linear programming and regularized least-squares methods are examples of pKa (i.e., −log Ka ) spectrum techniques that permit a quantitative assessment of surface chemical heterogeneity. Of the various modeling approaches, pKa spectroscopy is the most attractive because it does not require any a priori assumption about the number or nature of proton binding sites (Smith and Ferris 2001). In deriving a representative pKa spectrum for a sample, either a continuous or discrete model can be usefully applied depending on the needs of the investigator. Continuous pKa spectra are, nevertheless, more realistic for natural heterogeneous systems and are advantageous because it is possible to algebraically manipulate spectra in order to make comparisons between samples, such as in the comparison of individual end member spectra to the spectrum for composite sorbent materials (Martinez et al. 2002, 2003). A continuous binding model can be obtained using regularized nonlinear least-squares fitting (Smith and Ferris 2001). Regularized least-squares is like traditional least-squares with an added term corresponding to an a basic assumption about the system; i.e., that the pKa spectrum is a smooth continuous function. In applying the regularized least-squares technique, it is possible to optimize both the goodness-of-fit and the regularization function, i.e., smoothness. This involves minimization of the residual sum of squares error function (SS), as well as the regularization function (R) in SS-R space (Smith and Ferris 2001). The method, known as Fully Optimized ContinUouS (FOCUS) pKa spectroscopy, has been used to assess the chemical heterogeneity of mineral and bacterial cell surfaces, as well as BIOS composites. The FOCUS approach has been used to optimize acid base ¨ o HRL, and the corretitration data for intact BIOS from the Asp¨ sponding hydroxylamine insoluble bacterial fraction (Martinez et al. 2003). Then the FOCUS pKa spectrum obtained from the hydroxylamine insoluble bacterial cell fraction was subtracted from the intact BIOS pKa spectrum. This removed overlapping

2.4 HFO

2.0 Site Density (mmole / g)

fraction in the BIOS. When calculated solid phase Sr2+ values for the S. alga-ferrihydrite composite were plotted against measured values, a strong linear trend was observed; however, the plot was above and parallel to the 1:1 reference line indicating an overestimation of sorbed Sr2+ compared to the amount actually sorbed by the synthetic BIOS composite. This behavior is consistent with a masking of Sr2+ binding sites owing to chemical interactions between the bacterial cells and ferrihydrite in the composite (Martinez et al. 2003; Smith and Ferris 2003).

BIOS Bacteria

1.6 1.2 0.8 0.4 0.0

3

4

5

6

7

8

9

10

pKa FIG. 4. Reactive site density envelopes for intact BIOS, the hydroxylamine insoluble bacterial fraction, and corresponding HFO fraction determined from FOCUS pKa spectra. Arrows indicate (a) the higher density of acidic (i.e., low pKa) sites in the bacterial fraction, and (b) lower density of basic (i.e., high pKa) sites in intact BIOS.

pKa contributions from the bacteria to yield a residual deconvoluted pKa spectrum that portrayed conceptually the concentration and pKa distribution of proton binding sites present on the HFO portion of the BIOS (Martinez et al. 2003). Individual site densities for intact BIOS and each of the two end-member components are shown in Figure 4. The pKa reactivity profile for the BIOS and HFO are similar in the acidic to mid-pKa range; however, the concentration of high pKa sites is reduced in the BIOS compared to HFO (Martinez et al. 2003). Conversely, the hydroxylamine insoluble bacterial fraction is enriched in low pKa sites relative to both BIOS and HFO. These observations indicate that low pKa sites associated with bacteria in BIOS interact specifically with basic pKa sites on intermixed HFO (Smith and Ferris 2003), as inferred from the non additive metal binding behavior of bacteria-HFO composites synthesized in the laboratory (Small et al. 2001). The surface charge excess curves generated from the titrations revealed apparent point of zero charge (pHpzc ) values of 9.6 ± 0.1 for the BIOS and 4.1 ± 0.1 for the hydroxylamine insoluble bacterial fractions, respectively. These pHpzc values were estimated from the pH value where the surface charge excess was zero; however, it should be noted that these estimates are not directly equivalent to actual points of zero charge, which are by convention determined from a series of acid base titrations conducted at different ionic strengths (Smith and Ferris 2001; Martinez et al. 2002). Nevertheless, the bacterial cell fraction pHpzc of 4.1 ± 0.1 compares favorably with the value of 4.5 ± 0.1 reported for Gram-positive bacterial cell wall fragments (Plette et al. 1995). In turn, the pHpzc of 9.6 ± 0.1 for the BIOS equates well with values of 9.4 and 8.6 to 9.3 reported for goethite and hematite, respectively (Plette et al. 1995; Hiemstra and Van Riemsdijk 1996; Felmy and Rustad 1998). Collectively, these high pHpzc

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values suggest that BIOS surface charge is dominated by contributions from reactive groups associated with hydrous ferric oxide rather than bacterial cells in the composite. This implies further that the acidic (i.e., low pKa ) groups associated with and contributing to the low apparent pHpzc of the bacterial cell fraction interact chemically with hydrous ferric oxide, and thus are not subject to titration in composite BIOS samples (Warren and Ferris 1998; Smith and Ferris 2003). SUMMARY BIOS are composite materials that consist of intact and partly degraded remains of bacterial cells intermixed with variable amounts of poorly ordered HFO minerals. They are formed when chemical or bacterial oxidation of Fe2+ gives rise to Fe3+ , which then undergoes hydrolysis to precipitate in association with bacterial cells. While there is ample evidence showing that bacteria accelerate Fe2+ oxidation rates in acidic environments, only recently has this been affirmed in neutral pH systems under low pO2 conditions. Because of their broad distribution and reactive surface properties, BIOS are believed to play an important role in regulating the fate and behavior of dissolved metal ions; however, the metal sorption properties of BIOS are not additive owing to chemical surface chemical interactions between the constituent HFO and bacteria. The biogeochemical implications of HFO-bacterial interactions in BIOS remain to be fully explored, and are likely to be a major focus for future research. REFERENCES Anderson CR, Pedersen K. 2003. In situ growth of Gallionella biofilms and partitioning of lanthanides and actinides between biological material and ferric oxyhydroxides. Geobiol J 1:169–176. Bigham JM, Schwertmann U, Pfab G. 1996. Influence of pH on mineral speciation in a bioreactor simulating acid mine drainage. Appl Geochem 11:845– 849. Chan CS, De Stasio G, Welch SA, Girasole M, Frazer BH, Nesterova MV, Fakra S, Banfield JF. 2004. Microbial polysaccharides template assembly of nanocrystal fibers. Science 303:1656–1658. Cox JS, Smith DS, Warren LS, Ferris FG. 1999. Characterizing heterogeneous bacterial surface functional groups using discrete affinity spectra for proton binding. Environ Sci Technol 33:4514–4521. Dzombak DA, Morell FMM. 1990. Surface Complexation Modeling: Hydrous Ferric Oxides. New York: John Wiley and Sons, New York. p 89– 102. Edwards KJ, Rogers DR, Wirsen CO, McCollom TM. 2003. Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α- and γ -Proteobacteria from the Deep Sea. Appl Environ Microbiol 69:2906–2913. Edwards, KJ, Bach W, McCollom TM, Rodgers DR. 2004. Neutrophilic ironoxidizing bacteria in the ocean: their habitats, diversity, and roles in mineral deposition, rock alteration, and biomass production in the Deep Sea. Geomicrobiol J 21:393–404. Emerson D, Revsbech NP. 1994. Investigation of an iron-oxidizing microbial mat community located near Aarhus, Denmark: field studies. Appl Environ Microbiol 60:4022–4031. Emerson D, Moyer C. 1997. Isolation and characterization of novel ironoxidizing bacteria that grow at circumneutral pH. App Environ Microbiol 63:4784–4792.

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