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Siderophore-Manganese(III) Interactions. I. Air-Oxidation of Manganese(II) Promoted by Desferrioxamine B OWEN W. DUCKWORTH* AND GARRISON SPOSITO Division of Ecosystem Sciences, University of California, Berkeley, California 94720-3114
Recent studies suggest that aqueous Mn(III) complexes, particularly those with non-carboxylated ligands such as microbial siderophores, may be stable in soil and aquatic environments. In this paper, we determine the stability constants for Mn(II) and Mn(III) complexes with the common trihydroxamate siderophore, desferrioxamine B (DFOB). Base and redox titrations were conducted to determine DFOB conditional protonation constants and conditional stability constants for 1:1 DFOB complexes with Mn(II) and Mn(III). The conditional protonation constants agree well with literature values. We determined stability constants for three Mn(II)-DFOB species and one Mn(III)-DFOB species at 25 °C in 0.1 M NaCl. The Mn(III) HDFOB+ complex can be formed readily by air-oxidation of Mn(II)-DFOB. This reaction exhibits pseudo first-order kinetics with a rate coefficient that can be characterized as the product of oxygen concentration with a linear combination of the concentrations of the three Mn(II)-DFOB complexes. The second-order rate coefficients appearing in this linear combination are 1 to 2 orders of magnitude smaller than that associated with oxidation of the hydrolytic species Mn(OH)02. The Mn(III)HDFOB+ complex is stable for pH in the range of 7.0-11.3; but, at pH < 7.0 it decomposes by internal electron transfer, yielding oxidized DFOB products and Mn(II). For p[H+] > 11.3, the complex degrades by disproportionation, yielding Mn(II) and solid MnO2. This range of pH stability supports the hypothesis that aqueous Mn(III) may play a vital role in the biogeochemical cycling of not only manganese, but also other elements, such as carbon, sulfur, nitrogen, oxygen, and redox-active metals.
Introduction Siderophores are biologically produced, organic chelating ligands that strongly complex Fe(III) (1-3) and other hard metal ions (4, 5). Several studies have shown that siderophores form aqueous complexes with Mn(III) (6-9), an oxidation state that is normally unstable in aqueous solution (10). Faulkner et al. (7) identified a stable 1:1 complex composed of Mn(III) and desferrioxamine B (DFOB), a common trihydroxamate siderophore. This complex can be formed * Corresponding author phone: 510-643-9951; e-mail: owend@ nature.berkeley.edu. 10.1021/es050275k CCC: $30.25 Published on Web 07/12/2005
2005 American Chemical Society
by the oxidation of Mn(II) in Mn(II)-DFOB complexes or by the dissolution of Mn(III) oxides. Parker et al. (8) characterized a pyoverdine siderophore produced by the Mn(II)-oxidizing bacteria Pseudomonas putida MnB1 that exhibits a higher affinity for Mn(III) than for Fe(III). These recent observations suggest that Mn(III)-siderophore complexes may be persistent in natural environments and may influence the aqueous speciation of manganese, iron, and siderophores. Aqueous Mn(II) is thermodynamically unstable in alkaline oxic environments; however, its oxidation is kinetically sluggish at circumneutral pH, except when catalyzed by mineral surfaces (11-16), microbes (17), or high-affinity ligands (18). Siderophores complex bivalent metals at circumneutral pH and stabilize their higher oxidation states (4), potentially providing both a mechanism for Mn2+ oxidation in natural environments and a source of aqueous Mn(III) complexes. In this study, we employ DFOB, a trihydroxamate siderophore produced by Streptomyces pilosus (19), for several reasons: (1) the aqueous chemistry (1, 4) and dissolution reactivity (20, 21) are better understood than for other siderophores; (2) DFOB may serve as a model for a large class of siderophores, the trihydroxamates (22); and (3) it is commercially available, highly soluble, and stable over a wide pH range. Although several Mn(III)-siderophore complexes have been synthesized (6-9), the kinetics of environmentally relevant formation reactions have not been examined. These reactions may play a significant role in the cycling of manganese and other redox-active elements. In this study, we build on the pioneering work of Faulkner et al. (7) by measuring the stability constants of complexes formed by Mn(II,III) and DFOB, by determining the chemical conditions under which the complex is stable, and by studying the kinetics of DFOB-promoted Mn(II) oxidation.
Materials and Methods Materials. The sample of DFOB utilized in this study is the mesylate salt [(C25H46N5O8NH3+(CH3SO3)-] produced under the trade name Desferal. The sample was a gift from the Salutar Corporation. All solutions are made with deionized water with a resistivity of 18.3 MΩ-cm. Unless otherwise specified, all other chemicals are ACS reagent grade. The green Mn(III)HDFOB+ complex has an 310 ) 2060 ( 20 M-1 cm-1. The synthesis of this complex is discussed further in the Supporting Information. Titrations of Aqueous DFOB Complexes. Base titrations were conducted to determine DFOB conditional protonation constants (denoted generally as cK[HLm+1], where the subscript is the protonated product species, Lm is a weak acid, and the superscript c denotes that the constant is conditionally defined for a specific ionic strength) and conditional binding constants (denoted generally as cK[LMm+n], where the subscript is the associated product species and Mn is a metal ion) for Mn(II) and Mn(III) in 0.1 M NaCl (5, 23). Titrations were conducted in a 100-mL Pyrex lipless flask capped with a rubber stopper that was placed in a water bath at 25 °C. The stopper was fitted with ports to accommodate a glass electrode, a fritted-glass gas dispersion tube, a sample port, and a gas vent. The apparatus was vigorously purged with humidified N2 to stir the solution as well as to exclude atmospheric gases. To avoid ambiguities in the measurement of proton activity, the pH electrode was calibrated in terms of proton concentration (p[H+]) by measuring cell emf as a function of proton concentration by using commercially VOL. 39, NO. 16, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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standardized solutions of HCl and NaOH (Fisher) in 0.1 M NaCl (Fisher) (24). All titrations were conducted in triplicate. To determine conditional protonation constants, 100mL samples containing 0.1 M NaCl and 1 mM DFOB were titrated with 200-µL additions of standardized 0.1 M NaOH delivered by a calibrated micropipet. Solutions were purged for at least 1 h with humidified N2 before each experiment. With each addition, p[H+] was measured after equilibration by using an Orion Ross combination glass pH electrode connected to a Beckman Φ 71 pH meter. For all titrations, the system was assumed to be at equilibrium when no measurable change in cell emf ( 11.1 ( 0.2. Despite the reasonable agreement with our experimental value of p[H+] > 11.3, this calculation is limited, in that it does not account for the possible formation of the Mn(III)DFOB0 complex at pH > 10, analogous to Fe(III) (1). At low pH, Mn(III) complexes decompose by intramolecular electron transfer, yielding Mn(II) and oxidized ligand (18, 23, 41, 44). Aminopolycarboxylate-Mn(III) complexes typically degrade by internal electron transfer, with the ligand undergoing a decarboxylation reaction (23, 41). We find that the Mn(III)HDFOB+ complex also degrades by intramolecular electron transfer, based on the irreversible loss of the complex at pH < 7. Although the complex degrades irreversibly, a solution containing the oxidation products and Mn(II) develops a UV-visible spectrum similar to DFOB
if allowed to air-oxidize at alkaline pH for several hours. This observation suggests that the oxidation products form a stable complex with Mn(III) that has a chromophore similar to that in the Mn(III)HDFOB+ complex. Electrospray mass spectrometry was utilized to examine the identity of the degradation products of DFOB. Experimental details of sample preparation and analysis are provided in the Supporting Information. Our spectra of DFOB alone and of Mn(III)HDFOB+ (data not shown) agreed well with available literature spectra (7), except that we noted contamination by Al, Fe, and Ga in our DFOB sample, as identified by major isotopic peaks at m/z ) 585, 614, and 627. [Calculated isotopic signatures of Al(III)HDFOB+, Fe(III)HDFOB+, and Ga(III)HDFOB+ complexes agreed well with the peak patterns observed in the mass spectra.] The mass spectra of the samples containing degradation products and the complex of Mn(III) formed by these products did not show dominant products (data not shown), but instead showed many peaks with m/z ) 200-400. This result is consistent with the hydrolytic cleaving of DFOB observed during microbial degradation (45-48), except that the redox reaction in our study yields many different degradation products. The rate of internal reduction and the final [Mn(III)HDFOB+] are highly pH-dependent for pH < 7 (Figure 2). We describe the reaction by the putative overall oxidation reaction described as follows:
Mn(III)HDFOB+ + 3H+ f Mn2+ + Oxidized DFOB (14) Because we do not know the stoichometry or protonation of the products, we are unable to calculate the equilibrium constant for the reaction. It is important to note that the reaction in eq 14 is the irreversible oxidation of DFOB, not simply the reversible reduction of the metal center, as commonly observed for Fe(II)HDFOB0/Fe(III)HDFOB+ complexes using cyclic voltammetry (39). Modeling of Air-Oxidation of Mn(II)-DFOB Complexes. The Mn(II) oxidation rate is greatly enhanced by DFOB. Figure 4A shows the aqueous speciation of the oxidation-active Mn(II) species in a solution in equilibrium with atmospheric CO2 (log Pco2 ) -3.45) containing 0.1 NaCl, 1 mM Mn(II), and 1 mM DFOB, as calculated by using MINEQL+ (37). Below pH ) 10, the dominant species are Mn(II)-DFOB complexes. Using this calculated aqueous speciation, the optimization of the model presented in eq 11 yields kMn(II)DFOB- ) 10.7 M-1 s-1, kMn(II)HDFOB0 ) 0.62 M-1 s-1, and kMn(II)H2DFOB+ ) 0.21 M-1 s-1 for the Mn(II)-DFOB species. Figure 4B shows a log-log plot of the model kfit plotted against the experimental kT. The regression line yields a line with a slope of unity and a zero intercept, indicating that the model reproduces the data well over the pH range studied. An additional measure of the goodness of fit is provided by the residual of the optimization, ∑j (log kT - log kfit)j2. Our residual is 0.1972, a value comparable to the residual (0.31174) found by Morgan (35) for an equal number of experimental trials, indicating a reasonable fit to the data. On the basis of Morgan’s analysis (35), we estimate the error in the second-order rate coefficients as ∼25%. For all oxidation experiments, greater than 99.5% of the observed reactivity is accounted for by DFOB-Mn(II) complexes (data not shown). DFOB facilitates Mn(II) oxidation because at pH < 10 it forms stronger complexes with Mn(II) than common inorganic ligands. The efficacy of DFOB for promoting Mn(II) oxidation can be explained by noting that the ligand donates negative charge to the complexed Mn(II), which lowers the activation energy of the oxidation reaction and thus facilitates electron transfer from complexed Mn(II) to the O2 (35, 49). Ligands that preferentially stabilize higher valence states of metals also increase the thermodynamic force driving the oxidation reaction. This driving VOL. 39, NO. 16, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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response to iron stress (22), which is common under oxic to suboxic conditions at circumneutral pH, conditions that render iron virtually insoluble. Because manganese oxidation is less favorable kinetically than iron, Mn(II) concentrations are typically several orders of magnitude greater than the total iron concentration under these conditions (28). Therefore, siderophore production occurs typically under conditions that favor formation of Mn(III)HDFOB+ by oxidation of Mn2+. Manganese(III) complexes may play an important role in the geochemistry of natural waters. Manganese is directly involved in the redox chemistry of metals and the oxidation of organics at mineral surfaces (10). Aqueous complexes of Mn(III) can react in an analogous manner, oxidizing organics (6, 7, 18, 41, 64-66), metals (6, 65-67), sulfide (65), and nitrite (68). Additionally, for pH < 7, the siderophore can be oxidized internally by Mn(III), providing a potential pathway for the abiotic degradation of siderophores. This reactivity suggests that aqueous Mn(III) may play a vital role in the biogeochemical cycling of not only manganese, but also other elements, such as carbon, sulfur, nitrogen, oxygen, and redoxactive metals.
Acknowledgments
FIGURE 4. Kinetics modeling of Mn(II) oxidation. (A) Calculated speciation of DFOB species in a solution open to atmospheric CO2 (log Pco2 ) -3.45) containing 1 mM DFOB, 1 mM Mn(II), and 0.1 M NaCl using protonation and formation constants in Table 1 along with formation constants for inorganic Mn species from ref 35. The shaded regions indicate the uncertainty in the concentrations of the Mn(II)-DFOB species. The uncertainty was estimated by calculating the aqueous speciation while varying the KM within the range of the error presented in Table 1 and holding all other parameters constant. The calculations were performed by using MINEQL+ (37). (B) Modeled log[kfit] versus measured log[kT]. Solid lines represent best-fit regressions (R2 ) 0.99). Triangles, 0.5 mM DFOB and MnCl2. Diamonds, 0.25 mM DFOB and MnCl2. Conditions: 0.1 M NaCl, 5 mM buffer, 25 °C, open to the atmosphere. force correlates positively with the oxidation rate of Fe(II) (50, 51) and other metals (52). The formation constant of Mn(III)HDFOB+ exceeds that of the potentially active Mn(II)-DFOB complexes by approximately 22 orders of magnitude, thus providing a large thermodynamic driving force for the conversion of Mn(II)-DFOB complexes to Mn(III)HDFOB+. Environmental Implications. Previous work has suggested that stable aqueous Mn(III) complexes may exist in soil environments (53, 54) and natural waters (55). Several mechanisms exist for the formation of these complexes. Ligand-promoted dissolution of Mn(III,IV) phases can yield Mn(III) complexes (9, 56, 57). Biologically produced Mn may also provide a significant source of soluble Mn(III). The lysis of dead cells releases Mn(III)-containing enzymes, such as superoxide dismutase, acid phosphatase, redox enzymes (58), and photosystem II-related enzymes (59). These enzymes bind manganese with high affinity, suggesting that they may be persistent in the environment. Sugar residuals, such as gluconate (60), sorbitol (61), and mannitol (62), have been shown to form stable complexes with Mn(III) in laboratory studies. It is thus reasonable that microbially produced extracellular polysaccharides, a common component of exudates and biofilms (63), may also form stable Mn(III) complexes. The oxidation of Mn(II)-DFOB complexes introduces another pathway for the generation of aqueous Mn(III) complexes. Siderophores are exuded by microbes as a 6042
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We are grateful to Kenneth Raymond for providing our sample of Desferal. Tia Shimada graciously assisted in gel electrophoretic mobility experiments. We thank Ulla N. Anderson for assistance in interpreting mass spectra. We thank Jasquelin Pen ˜ a and Brandy Toner for valuable discussion, and Edward Bellfield and Andrew Yang for logistical support. This work was funded by the National Science Foundation, Collaborative Research Activities in Environmental Molecular Science (CRAEMS) program (grant CHE-0089208).
Supporting Information Available Descriptions of additional experimental procedures, tabulated kinetic data, and calculated aqueous speciation data. This material is available free of charge via the Internet at http://pubs.acs.org.
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Received for review February 10, 2005. Revised manuscript received June 1, 2005. Accepted June 7, 2005. ES050275K
