Nutrient Effect on the Biological Leaching of a Black-Schist Ore
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1 PPLIED ND ENVIRONMENTL MICROBIOLOCY, pr. 1994, p Vol. 6, No /94/$4.) + Copyright 1994, merican Society for Microbiology Nutrient Effect on the Biological Leaching of a Black-Schist Ore SEPPO I. NIEMEL,' MRJ RIEKKOL-VNHNEN,- CRIT SIVEL,' FELIPE VIGUER,'t ND OLLI H. TUOVINEN3* Department of pplied Chemistry and Microbiology, FIN-14 University of Helsinki, and Outokumpai Research Oy, FIN-2811 Pori,2 Finland, and Department of Microbiology, The Ohio State University, Columbus, Ohio Received 12 October 1993/ccepted 28 January 1994 The purpose of the study was to examine the influence of inorganic N (NH4', NO3 -) and phosphate on the biological oxidation of a sulfidic black-schist ore which contained pyrrhotite as the main iron sulfide. Iron was initially solubilized as Fe2+ from the ore and subsequently oxidized to Fe3+ in shake flask experiments. Under these experimental conditions, iron dissolution from pyrrhotite was mainly a chemical reaction, with some enhancement by bacteria, whereas the subsequent Fe2+ oxidation was bacterially mediated, with negligible contribution from chemical oxidation. osphate amendment did not enhance Fe2+ oxidation. Chemical analysis of leach solutions with no exogenous phosphate revealed that phosphate was solubilized from the black-schist ore. mmonium amendment (6 mm) enhanced Fe2+ oxidation, whereas the addition of nitrate (6 and 12 mm) had a negative effect. n increase in the temperature from 3 to 35 C slightly enhanced Fe2+ oxidation, but the effect was statistically not significant. The precipitation of potassium jarosite was indicative of Fe2+ oxidation and was absent in nitrate-inhibited cultures because of the lack of Fe2+ oxidation. The black-schist ore also contained phlogopite, which was altered to vermiculite in iron-oxidizing cultures. Mesophilic chemoautotrophic bacteria (Leptospirillulm ferrooxidans, Thiobacillus ferrooxidans, Thiobacillus thiooxidants) involved in biological leaching processes require only inorganic nutrients for growth with ferrous iron and sulfur compounds (6, 12). Some of the major and minor nutrient requirements, e.g., P, K, Mg, and trace metals, may be met with mineral constituents dissolved from ores during biological leaching processes. In contrast, the dissolution of minerals as a nutrient source represents a minor contribution to satisfy the cellular N requirement. mmonium appears to be the preferred source of N for chemoautotrophic, acidophilic thiobacilli. The ability of these bacteria to assimilate nitrate is variable as is also the ability to fix No (13, 14). Therefore, N amendment of leach solutions may enhance biological activities in leaching systems. The purpose of the present study was to examine the influence of ammonium N, nitrate N, and phosphate P amendment on the biological leaching of a black-schist ore. The sample contained pyrrhotite (Fe,,S) as the main source of Fe(II), which was dissolved as Fe2+ and biologically oxidized to Fe"3. MTERILS ND METHODS The black-schist ore contained pyrrhotite (Fe1,S), pyrite (FeS,), sphalerite (ZnS), pentlandite [(Ni,Fe,Co),S], and chalcopyrite (CuFeS2). Micas (primarily phlogopite), anorthite, microcline, and quartz were the main Si-containing phases. On the basis of elemental analyses (1) of a bulk sample, the following approximate composition was calculated: SiO-, 43.1 %; 123, 1.25%; Fe23, 23.2%; MgO, 3.4Cc; CaO, 2.13%; NaO,.27%; K,O, 4.87%; MnO,.39%; TiO, 1.65%; * Corresponding author. Mailing address: Department of Microbiology, The Ohio State University, 484 W. 12th ve., Columbus, OH Telephone: (614) Fax: (614) Electronic mail address: otuovine@( magnus.acs.ohio-state.edu. t Present address: Outokumpu Tecnica Chile Ltda., Santiago 9, Chile S 9-9%; P25,.11%. The sample was ground to a mesh (<59-pLm) particle-size fraction. mixed bacterial culture designated SB/P-II was used in the experiments. The culture was originally derived from composite mine water samples which were enriched with black-schist ore material as the sole energy substrate. Separate growth experiments established that the culture was a mixture of ferrous iron- and sulfur-oxidizing acidophilic bacteria. T. ferrooxidans was a major constituent in this consortium. The culture was routinely maintained with 5% (wt/vol) ore material in a mineral salts solution [2.3 mm K2HPO4, 3. mm (NH4)2SO4, 1.6 mm MgSO4 * 7H,O (ph 2)] at 28 C. The effect of nutrients (N and P) was investigated in four separate experiments which were carried out at different times. Two of these (experiments 1 and 4) were carried out at 3'C, and two (experiments 2 and 3) were carried out at 35 C. The basal salts medium was 1.6 mm MgSO4 * 7H2O (ph 1.5) supplemented with 5% (wt/vol) black schist. For inoculation, SB/P-Il was grown with the black-schist ore, harvested by centrifugation, washed, and resuspended in.5 M H2S4. The size of the inoculum was 5% (vol/vol), and its density was -5 x 17 bacteria per ml after inoculation. Control flasks (sterilized by autoclaving) received 5% (vol/vol) sterile 5 mm H2SO4. The test nutrients were, 2.8, and 5.4 mm phosphate - (added as KH2PO4 3H2), and 6. mm ammonium [added as (NH4)2SO4], and, 6.1, and 12.1 mm nitrate (added as NaNO3). The levels of phosphate and ammonium were selected to approximate their respective concentrations in the standard mineral salts medium. n ammonium-free mineral salts solution was also used, and nitrate at a comparable level and nitrate at a twofold-higher level were included as references. For P, the two other levels were chosen to represent conditions of (i) no exogenous addition and (ii) phosphate excess. No effort was made to optimize the N and P levels in the mineral salts medium before these experiments were performed. The cultures were prepared in duplicate and incubated in shake flasks at 18 rpm. Because of pyrrhotite dissolution and iron oxidation, the net reaction was initially
2 1288 NIEMEL ET L. PPL. ENVIRON. MICROBIOL. I-, LLE -o u) U) U) 1 2+ ~Fe, 3+ Fet.t., /\, Time (days) FIG. 1. Dissolution of black-schist ore (5% [wt/vol]) in a chemical control containing magnesium sulfate in 5 mm H2SO4. The experiment was carried out at 3C. acid consuming, raising the ph from 1.5 to 2. to 2.4 depending on the composition of the mineral salts medium. Subsequent ferric iron hydrolysis and the oxidation of pyrite were acidproducing reactions and decreased the ph to 1.8 to 2.1. The concentrations of ferrous iron (Fe2+) and total dissolved iron (Fet,,tai) in solution were determined with the o-phenanthroline method (7, 1). The concentrations of ferric iron (Fe3+) in solution was derived by calculation (Fetltal - Fe2+). Residual ammonium concentrations in leach solution samples in experiment 4 were determined with an ion-specific electrode. Dissolved phosphate was determined colorimetrically with ammonium molybdate (9). The data were analyzed with multiple regression, with concentrations of Fe2' and Fe3+ as response variables and time, temperature, phosphate, and different forms and concentrations of N as predictor variables. Regression analysis was followed by factorial analysis of variance separately for the data of days 2, 4, and 7 of the experiment. Computations were made with Statistix II computer software (NH nalytical Software, Roseville, Minn.). Logarithmic transformation of the data was necessary to normalize the response variables. Mineralogical composition of leach residues from experiment 4 was analyzed by x-ray diffraction (XRD). Leach residue samples were recovered by centrifugation, washed, air dried, and gently ground in a mortar. XRD analyses of powder mounts were conducted with a Siemens D5 diffractometer, using CuKoL radiation and a wide-range goniometer equipped with a diffracted-beam monochromator and a compensating slit. The specimens were scanned from 6 to 72 in increments of.52 with a 1-s step time. The XRD analysis of the untreated black-schist ore was conducted by using a 4-s step time (ilips PW 1316/9 system). RESULTS ND DISCUSSION measured as the concentration of Fet,tal, Iron dissolution, commenced with a minimum lag period. comparison of the sterile control and inoculated system revealed that pyrrhotite dissolution was primarily abiotic during the first few days of contact with leach solution (Fig. 1 and 2). The increase in total iron concentration was linear at the beginning of the time course. The initial increase in the Fe2+ concentration was due to the solubilization of the relatively high pyrrhotite content. In the first few days, Fe2+ accounted for most of the Fet tai in leach solutions. This pattern of iron dissolution is characteristic of nonoxidative leaching of pyrrhotite: Fej,S + 2H+ -> (1-3x)Fe2+ + 2xFe3+ + H2S (1) I a, E a 2 1) IU- \ 1-1 U) L.L -, E + ru Li Time (days) FIG. 2. Changes in the concentrations of FetlIal (), Fe2+ (B), and Fe3+ (C) during bacterial leaching of black-schist ore (5% [wt/vol]) in experiment 4 (3 C) with addition of 2.8 mm phosphate. The Fe1-xS formula of pyrrhotite represents a nonstoichiometric, Fe-deficient sulfide of varying composition (11) and with a minor component of Fe(III). Previously, it has been shown that pyrrhotite is solubilized faster than the other sulfide minerals present in this black-schist ore (4, 5). Oxidative dissolution of pyrrhotite to Fe2+ with subsequent oxidation to Fe3+ is accompanied by the concomitant production of elemental S: 4Fel,S H+ -* (4-12x)Fe2+ + &xfe3+ + 4S + 4H2 (2) 4Fel,S + (3-3x)2 + (12-12x)H+ -> (4-4x)Fe3+ + 4S + (6-6x)H2 (3) 4Fe H+ -+ 4Fe3+ + 2H2 (4) The acid-consuming phase of pyrrhotite leaching and the formation of elemental S have been demonstrated previously in bacterial oxidation experiments with research-grade pyrrhotite (3). The extent of iron dissolution varied depending on the nutrient amendment. In general, the highest Fetotal levels were present in culture flasks that received 12 mm nitrate (Fig. 2). Iron oxidation varied depending on the treatment. Comparable results were obtained in the four experiments, except for
3 VOL. 6, 1994 NUTRIENT EFFECT ON BIOLOGICL LECHING 1289 TBLE 1. Summary of stepwise regression analysis of Fe data (n = 64) after 2 days of incubation In [Fe2+Ia In [Fe3+]b In ([Fe2+]/[Fetota])c In ([Fe3+]/[Fetotail)d Constant < Temp ( C).1116 < N3- (mm) NH4+ (mm) osphate (mm) a R2 = br2 = cr2 =.16. d R2 =.37. differences in (i) the lag periods preceding Fe2+ oxidation and (ii) the relative degree of inhibition of Fe2+ oxidation in the nitrate-amended test cultures. Ferrous iron oxidation was particularly enhanced in the NH4'-supplemented culture (Fig. 2). Cultures that were not amended with an external nitrogen source also oxidized Fe2+ faster than those amended with either 6 or 12 mm nitrate (Fig. 2). Nitrate toxicity was apparent in these experiments. T. ferrooxidans and other chemoautotrophic acidophiles are particularly sensitive to nitrate and other anions because of their nonspecific permeability and, especially, intracellular accumulation driven by transmembrane potential, t (2, 8). Nitrate inhibition is associated with acidification of the cytoplasm because the change in t is balanced by proton entry (2). nalysis of variance was used initially to identify effective variables. It indicated a significant interaction between N addition and the temperature of incubation. The reason for this interaction was the positive enhancement of Fe2+ oxidation by NH4' addition and the negative effect caused by the addition of NO3-. No other statistically significant main effects or interactions were seen between the experiment, duplicate culture, temperature, N addition, or phosphate addition. Repeatability (relative standard deviation) of the analytical determinations of Fe2' and Fe3", based on the residual (between-flask) variance, was generally of the order of ±35% when back-transformed to arithmetic scale. Linear regression analyses of the data revealed that the incubation time, temperature, nitrate, and ammonium had significant effects on Fe2' dissolution, Fe3+ oxidation, and fractional concentrations of ferrous (Fe2+/Fetotal) and ferric (Fe3+/Fetotal) iron. The effects of ammonium and nitrate had opposite effects on Fe2+ oxidation because ammonium enhanced and nitrate inhibited Fe2+ oxidation. osphate amendment was without an effect. This lack of effect was attributed to phosphate dissolution from the black-schist ore. Most of the data sets indicated that temperature had a negative effect on Fe2" concentration and a positive effect on Fe3" concentration, suggesting that the increase from 3 to 35 C resulted in faster Fe2+ oxidation rates. These observations are quite evident in the series of regression models fitted to the data after 2, 4, and 7 days of incubation. fter 2 days of incubation (Table 1), hardly any sign of biological activity was detected, and the coefficients of regression (R2) were low. The only response seemed to be an increase in Fe2` due to pyrrhotite dissolution from the ore. fter 4 and 7 days (Tables 2 and 3), biological effects such as significant nutrient effects on pyrrhotite dissolution and Fe2+ oxidation and changes in fractions of Fe2+/Fetotal and Fe3+/ Fetotai, with resulting increases in the R2 values of the regression models, were clearly discerned. The significant effect caused by the temperature is in strong support of the interpretation that these responses were due to biological activity. The data in Fig. 2 are consistent with these conclusions. mmonium and phosphate were analyzed in leach solutions at the conclusion of experiment 4. These results are presented in Table 4. mmonium levels were generally '.6 mm, except for an anomaly in one sample (2.4 mm NH4+) that had received ammonium amendment but no phosphate. The low NH4' levels in ammonium-amended cultures were taken to represent a combination of cellular assimilation and precipitation of ammonium jarosite. The residual phosphate concentrations in leach solutions ranged between.2 and 4.9 mm (Table 4). In general, the higher levels were consistent with the higher initial addition of phosphate at the beginning of the experiment. Without external addition, the residual phosphate levels in leach solutions were in the range of.6 to 1.2 mm, reflecting partial solubilization of the.11% P25 content of the black-schist ore during leaching. XRD analysis of untreated black-schist ore (Fig. 3) revealed TBLE 2. Summary of stepwise regression analysis of Fe data (n = 64) after 4 days of incubation In [Fe2+11 In [Fe3+]b In ([Fe2+]/[Fe,o,a1I)c In ([Fe3+]/[Fetotai])d Constant < <.1 Temp ( C) < <.1 NO3- (mm) NH4+ (mm) < < < <.1 osphate (mm) a R2 = b R2 = cr2 =.81. d R2 =.544.
4 129 NIEMEL ET L. PPL. ENVIRON. MICROBIOL. TBLE 3. Summary of stepwise regression analysis of Fe data (n = 64) after 7 days of incubation In [Fe2+]a In [Fe3+] In ([Fe2+]/[Feto,ai])c In ([Fe3+]/[Fet,,ta])d Constant < <.1 Temp ( C) < < NO3- (mm).1283 < NH4+ (mm) < osphate (mm) a 2= b R2 = cr2=.721. d R2 = diffraction lines for major and minor sulfide minerals (pyrrhotite, pyrite, pentlandite, sphalerite, chalcopyrite) as well as for graphite and for Si-containing solid phases (quartz, phologopite, microcline, anorthite, chlorite). s indicated in Fig. 3, some XRD lines of several minerals overlapped each other. lthough the bulk ore sample contained.11% P25, phosphate minerals were not detected by XRD in untreated ore samples, suggesting that they were below the level of detection (< 2%). The XRD data showed that after contact with bacteria and the leach solution, jarosite [(K,NH4)Fe3(SO4)2(OH)6] was the main solid phase containing Fe(I11). Jarosite was formed both in unamended and NH4+-amended cultures, but it was not detected in cultures that received nitrate (Fig. 4). The XRD lines for pentlandite, sphalerite, and chalcopyrite could not be discerned with certainty because of overlap with lines for other minerals, but in general there was a reduction in the number and intensity of corresponding peaks. The pattern and yields of dissolution of Ni2+, Zn2+, Co2+, and Cu2+ have been discussed previously (4) and were not within the scope of the present work. Diffraction peaks of elemental S were detected in all solid residue samples, in keeping with the formation of elemental S from pyrrhotite under abiotic and biotic conditions (3, 4). Only traces of pyrrhotite were detected in leach residues, especially in those samples that had received either NH4+ or no N addition. While elemental S was present under all conditions, the NH4+-treated culture contained the least amount of it. These XRD data suggested that sulfur oxidation was enhanced in the presence of NH4+. The same culture also had the most jarosite. logopite [general formula, KMg3(Si3O1)(OH)2] was partially altered to a vermiculitetype structure in cultures that actively oxidized Fe2+. logopite alteration and vermiculite formation were not evident, and the XRD lines for pyrite and pyrrhotite were still present in leach residues from nitrate-amended cultures. The reduction in intensity of anorthite XRD lines suggested partial dissolution of this calcium feldspar. The relative proportion of quartz increased in some samples at the expense of the sulfide phases (Fig. 4 and B). The mineralogical observations indicated that K was stripped from the interlayer regions of the trioctahedral mica and that subsequent replacement of K by hydrated cations yielded an expansible mice phase, vermiculite. With concurrent bacterial oxidation of Fe2" to Fe3", K released from the interlayer was precipitated as potassium jarosite. Potassium jarosite was the predominant jarosite because of the excess K that was available from the weathering of phlogopite. Potassium jarosite was formed in the absence of N amendment, evidence for release of K from the mineral matrix in the black-schist ore. Compared with the NH4+-amended cultures, the XRD data indicated less oxidation of elemental S in the absence of added N, and thus less sulfuric acid was produced, resulting in a higher ph at the conclusion of the experiment. The lack of N extended the lag periods by a couple of days, and the Fetotal levels remained lower than those in the other,g, TBLE 4. Concentrations of residual ammonium and phosphate in leach solutions at the conclusion of experiment 4 Initial addition Nutrient concn (mm) Nitrogen osphate NH4+ P None None.6.6 None 2.8 mm None 5.4 mm mm NH4' None mm NH mm mm NH mm mm NO3-2.8 mm mm NO3 5.4 mm mm NO3-2.8 mm mm NO3-5.4 mm Degrees 29 CuKa p P FIG. 3. X-ray diffractogram of untreated black-schist ore. Symbols:, anorthite; Cp, chalcopyrite; C, chlorite; G, graphite; M, microcline; P, pyrrhotite;, phlogopite; PI, pentlandite; Pt, pyrite;, quartz; ZnS, sphalerite.
5 VOL. 6, 1994 NUTRIENT EFFECT ON BIOLOGICL LECHING 1291 D < P \l P CKNOWLEDGMENTS We thank U. Soto and J. M. Bigham for help in XRD data acquisition and interpretation. Partial funding of the work was received from Outokumpu Research Oy and the Nordisk Industrifond. This study is part of a cooperative project (O.H.T.) sponsored by the Division of International Projects of the National Science Foundation (INT ). C B v G M p P ~~~~~ JJ p \ J \f /M t V~~~~~, v \ G M i Dere 29 CuKa JJ J Degrees 2E) CuKaz FIG. 4. X-ray diffractogram of leach residues from experiment 4 (3 C) with addition of 2.8 mm phosphate. () No nitrogen amendment; (B) 6. mm NH4' amendment; (C) 6.1 mm NO3 - amendment; (D) 12.1 mm NO3- amendment. Symbols:, anorthite; G, graphite; J, jarosite; M, microcline; P, pyrrhotite;, phlogopite; Pt, pyrite;, quartz; S, elemental S; V, vermiculite. cultures. On the basis of the solution chemistry and XRD data, the lower Fetotal concentrations, with Fe3 as the predominant form in solution, can be taken to indicate extensive jarosite precipitation rather than limited dissolution of the primary iron sulfide, pyrrhotite. Jarosite saturation conditions in these biological leaching experiments are complex because of relatively fast kinetics of several concurrent reactions influencing ion activities. The results demonstrate that nutrient amendment indirectly influences the formation of solid phases in biological leaching processes. When bacteria actively oxidized Fe +, the mica (phlogopite) was altered to an expansible phase with a vermiculite structure as the weathering product. It is possible that potassium jarosite precipitation associated with the bacterial oxidation of Fe2+ constituted a sink for K which shifted the equilibrium toward the release of interlayer K from the mica phase (4), thereby resulting in structural alteration of phlogopite. REFERENCES 1. honen, L., and. H. Tuovinen Bacterial oxidation of sulfide minerals in column leaching experiments at suboptimal temperatures. ppl. Environ. Microbiol. 58: lexander, B., S. Leach, and W. J. Ingledew The relationship between chemiosmotic parameters and sensitivity to anions and organic acids in the acidophile Thiobacillus ferrooxidans. J. Gen. Microbiol. 133: Bhatti, T. M., J. M. Bigham, L. Carlson, and. H. Tuovinen Mineral products of pyrrhotite oxidation by Thiobacillus ferrooxidans. ppl. Environ. Microbiol. 59: Bhatti, T. M., J. M. Bigham,. Vuorinen, and. H. Tuovinen Weathering of mica and feldspar associated with the microbiological oxidation of pyrrhotite and pyrite, p In C. N. lpers and D. W. Blowes (ed.), Environmental geochemistry of sulfide oxidation. merican Chemical Society, Washington, D.C. 5. Bhatti, T. M., J. M. Bigham,. Vuorinen, and. H. Tuovinen Weathering of mica minerals in bioleaching processes, p In. E. Torma, J. E. Wey, and V. I. Lakshmanan (ed.), Biohydrometallurgical technologies, vol. I. Bioleaching processes. The Minerals, Metals & Materials Society, Warrendale, Pa. 6. Ewart, D. K., and M. N. Hughes The extraction of metals from ores using bacteria. dv. Inorg. Chem. 36: Herrera, L., P. Ruiz, J. C. guillon, and. Fehrmann new spectrophotometric method for the determination of ferrous iron in the presence of ferric iron. J. Chem. Technol. Biotechnol. 44: Ingledew, W. J cidophiles, p In C. Edwards (ed.), Microbiology of extreme environments. Open University Press, Milton. Keynes, United Kingdom. 9. Jeffery, G. H., J. Bassett, J. Mendham, and R. C. Denney Vogel's textbook of quantitative chemical analysis, 5th ed. Longman Scientific & Technical, Essex, United Kingdom. 1. Muir, M. K., and T. N. ndersen Determination of ferrous iron in copper-process metallurgical solutions by the o-phenanthroline colorimetric method. Metall. Trans. 8B: Nicholson, R. V., and J. M. Scharer Laboratory studies of pyrrhotite oxidation kinetics, p In C. N. lpers and D. W. Blowes (ed.), Environmental geochemistry of sulfide oxidation. merican Chemical Society, Washington, D.C. 12. Rossi, G Biohydrometallurgy. McGraw-Hill Book Co. GmbH, Hamburg, Germany. 13. Stevens, C. J., P. R. Dugan, and. H. Tuovinen cetylene reduction (nitrogen fixation) by Thiobacillusferrooxidans. Biotechnol. ppl. Biochem. 8: Stevens, C. J., and. H. Tuovinen Ferrous ion oxidation, nitrogen fixation (acetylene reduction), and nitrate reductase activity by Thiobacillus ferrooxidans, p In R. G. L. Mc- Cready (ed.), Proceedings of the Second nnual General Meeting of BIOMINET. CNMET Special Report SP85-6. Canada Centre for Mineral and Energy Technology, Ottawa, Ontario.
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