Abstract
We develop a comprehensive biogeochemical framework for understanding and quantitatively evaluating metals bio-protection in sulfidic microbial systems. We implement the biogeochemical framework in CCBATCH by expanding its chemical equilibrium and biological sub-models for surface complexation and the formation of soluble and solid products, respectively. We apply the expanded CCBATCH to understand the relative importance of the various key ligands of sulfidic systems in Zn detoxification. Our biogeochemical analysis emphasizes the relative importance of sulfide over other microbial products in Zn detoxification, because the sulfide yield is an order of magnitude higher than that of other microbial products, while its reactivity toward metals also is highest. In particular, metal-titration simulations using the expanded CCBATCH in a batch mode illustrate how sulfide detoxifies Zn, controlling its speciation as long as total sulfide is greater than added Zn. Only in the absence of sulfide does complexation of Zn to biogenic organic ligands play a role in detoxification. Our biogeochemical analysis conveys fundamental insight on the potential of the key ligands of sulfidic systems to effect Zn detoxification. Sulfide stands out for its reactivity and prevalence in sulfidic systems.
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References
Allen HE, Hansen DJ (1996) The importance of trace metal speciation to water quality criteria. Water Environ Res 68(1):42–53
Banaszak JE, van Briesen JM, Rittmann BE, Reed DT (1998) Mathematical modeling of the effects of aerobic and anaerobic chelate biodegradation on actinide speciation. Radiochim Acta 82:445–451
Barnes LJ, Jansen FJ, Scheeren PJH, Versteegh JH, Koch RO (1991) Simultaneous microbial removal of sulfate and heavy metals from wastewater. Paper presented at the 1st European Metals Conference, Bruxelles, Belgium
Benner SG, Blowes DW, Gould WD, Herbert RB Jr, Ptacek CJ (1999) Geochemistry of a permeable reactive barrier for metals and acid mine drainage. Environ Sci Technol 33(16):2793–2799
Brown PL, Markich SJ (2000) Evaluation of the free ion activity model of metal-organism interaction: extension of the conceptual model. Aquatic Toxicol 51:177–194
Campbell PGC (1995) Interactions between trace metals and organisms: critique of the free-ion activity model. In: Tessier A, Turner D (eds) Metal speciation and bioavailability in aquatic systems. Wiley, Chichester, UK
Campbell PGC, Errecalde O, Fortin C, Hiriart-Baer VP, Vigneault B (2002) Metal bioavailability to phytoplankton—applicability of the biotic ligand model. Comp Biochem Physiol Part C 133:189–206
Christensen BE, Characklis WG (1990) Physical and chemical properties of biofilms. In: Characklis WG, Marshall KC (eds) Biofilms. Wiley, New York
Cox JS, Smith DS, Warren LA, Ferris FG (1999) Characterizing heterogeneous bacterial surface functional groups using discrete affinity spectra for proton binding. Environ Sci Technol 33(24):4514–4521
Daskalakis KD, Helz GR (1993) The solubility of sphalerite (ZnS) in sulfidic solutions at 25°C and 1 atm pressure. Geochim Cosmochim Acta 57:4923–4931
Davies DG (1999) Regulation of matrix polymer in biofilm formation and dispersion. In: Wingender J, Neu TR, Flemming HC (eds) Microbial extracellular polymeric substances: characterization, structure and function. Springer-Verlag Berlin Heidelberg
De Filippi LJ (2000) Sulfate-reducing bacteria and other biological agents for bioremediation of hexavalent chromium and other heavy metals. In: Wise LW (ed) Bioremediation of contaminated soils. Marcel Dekker, New York
Dzombak DA, Morel FMM (1990) Surface complexation modeling. John Wiley & Sons, New York
Fein JB, Martin AM, Wightman PG (2001) Metal adsorption onto bacterial surfaces: development of a predictive approach. Geochim Cosmochim Acta 65:4267–4273
Fenchel T, Finlay BJ (1995) Ecology and evolution in anoxic worlds. Oxford University Press, New York
Flemming HC, Wingender J (2001) Relevance of microbial extracellular polymeric substances (EPSs)-Part I: structural and ecological aspects. Water Sci Technol 43(6):1–8
Gambrell RP (1994) Trace and toxic metals in wetlands-a review. J Environ Qual 23:883–891
Grady CPL Jr, Daigger GT, Lim HC (1999) Biological wastewater treatment, 2nd edn. Marcel Dekker Inc, New York
Guiné V, Spadini L, Sarret G, Muris M, Delolme C, Gaudet JP, Martins JMF (2006) Zinc sorption to three Gram-negative bacteria: combined titration, modeling, and EXAFS study. Environ Sci Technol 40:1806–1813
Hsieh KM, Murgel GA, Lion LW, Shuler ML (1994) Interactions of microbial biofilms with toxic trace metals 1. Observation and modeling of cell growth, attachment, and production of extracellular polymer. Biotechnol Bioeng 44:219–231
Kim CS, Zhou QH, Deng BL, Thornton EC, Xu HF (2001) Chromium(VI) reduction by hydrogen sulfide in aqueous media: stoichiometry and kinetics. Environ Sci Technol 35:2219–2225
Kuo WC, Parkin GF (1996) Characterization of soluble microbial products from anaerobic treatment by molecular weight distribution and nickel-chelating properties. Water Res 30(4):915–922
Laspidou CS, Rittmann BE (2002a) A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass. Water Res 36:2711–2720
Laspidou CS, Rittmann BE (2002b) Non-steady state modeling of extracellular polymeric substances, soluble microbial products, and active and inert biomass. Water Res 36:1983–1992
Liu H, Fang HHP (2002) Characterization of electrostatic binding sites of extracellular polymers by linear programming analysis of titration data. Biotechnol Bioeng 80(7):806–911
Lloyd JR, Mabbett AN, Williams DR, Macaskie LE (2001) Metal reduction by sulfate-reducing bacteria: physiological diversity and metal specificity. Hydrometal 59:327–337
Madigan MT, Martinko JM, Parker J (2000) Brock biology of microorganisms, 9th edn. Prentice-Hall, New Jersey
Morel FFM, Hering JG (1993) Principles and applications of aquatic chemistry. John Wiley & Sons, New York
Nielsen PH, Jahn A, Palmgren R (1997) Conceptual model for production and composition of exopolymers in biofilms. Water Sci Technol 36:11–19
NIST (1998) Critically selected stability constants of metal complexes database, Version 5.0
Noguera DR, Araki N, Rittmann B (1994) Soluble microbial products (SMP) in anaerobic chemostats. Biotechnol Bioeng 44:1040–1047
Paquin PR, Gorsuch JW, Apte S et al (2002) The biotic ligand model: a historical overview. Comp Biochem Physiol Part C 133:3–35
Rittmann BE, van Briesen JM (1996) Microbiological processes in reactive transport modeling. Rev Mineral 34:311–334
Rittmann BE, McCarty PL (2001) Environmental biotechnology: principles and applications. McGraw-Hill, New York
Rittmann BE, Banaszak JE, Reed DT (2002a) Reduction of Np(V) and precipitation of Np(IV) by an anaerobic microbial consortium. Biodegrad 13:329–342
Rittmann BE, Banaszak JE, Van Briesen JM, Reed DT (2002b) Mathematical modeling of precipitation and dissolution reactions in microbiological systems. Biodegrad 13:239–250
Rickard D (1995) Kinetics of FeS precipitation: Part 1. Competing reaction mechanisms. Geochim Cosmochim Acta 59(21):4367–4379
Sani RK, Peyton BM, Brown LT (2001) Copper-induced inhibition of growth of Desulfovibrio desulfuricans G20: assessment of its toxicity and correlation with those of zinc and lead. Appl Environ Microbiol 67(10):4765–4772
Schwarz AO, Rittmann BE (2006) Analytical-modeling analysis of how pore-water gradients of toxic metals confer community resistance. Adv Water Res (in press)
Schwarz AO, Rittmann BE (2007) Modeling bio-protection and the gradient resistance mechanism using CCBATCH. Biodegrad (in press). DOI 10.1007/s10532-007-9106-x
Songkasiri W, Reed DT, Rittmann BE (2002) Biosorption of neptunium(V) by Pseudomonas fluorescens. Radiochim Acta 90:785–789
Songkasiri W (2003) Biological processes in nuclear waste treatment: bio-sorption and bio-reduction of actinides. Dissertation, Northwestern University
Songkasiri W, Willett A, Reed DT, Rittmann BE, Koenigsberg S (2004) Bioremediation of neptunium(V) using lactate, hydrogen (H2), or hydrogen release compound (HRC). In: Proceedings of the 2003 Battelle symposium on in situ and on site bioremediation, Orlando, FL, June 2003
Stone AT (1997) Reactions of extracellular organic ligands with dissolved metal ions and mineral surfaces. Rev Mineral 35:309–344
Stumm W, Morgan JJ (1996) Aquatic Chemistry. John Wiley & Sons, New York
Sutherland IW (1999) Biofilm polysaccharides. In: Wingender J, Neu TR, Flemming HC (eds) Microbial extracellular polymeric substances: characterization, structure and function. Springer-Verlag Berlin Heidelberg
Sutherland IW (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiol 147:3–9
Tebo BM, Obraztsova AY (1998) Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol Lett 162:193–198
Van Briesen JM, Rittmann BE (1999) Modeling speciation effects on biodegradation in mixed metal/chelate systems. Biodegradation 10(5):315–330
Van Briesen JM, Rittmann BE (2000) Mathematical description of microbiological reactions involving intermediates. Biotechnol Bioeng 67(1):35–52
Van Briesen JM, Rittmann BE, Xun L, Girvin DC, Bolton H Jr (2000) The rate-controlling substrate of nitrilotriacetate for biodegradation by Chelatobacter heintzii. Environ Sci Technol 34:3346–3353
White C, Gadd GM (1998) Reduction of metal cations and oxyanions by anaerobic and metal-resistant microorganisms: chemistry, physiology, and potential for the control and bioremediation of toxic metal pollution. In: Horikoshi K, Grant WD (eds) Extremophiles: microbial life in extreme environments. Wiley & Sons, New York
Webb JS, McGinness S, Lappin-Scott HM (1998) Metal removal by sulfate-reducing bacteria from natural and constructed wetlands. J Appl Microbiol 84:240–248
White C, Sharman AK, Gadd GM (1998) An integrated microbial process for the bioremediation of soil contaminated with toxic metals. Nat Biotechnol 16:572–575
Widdel F (1988) Microbiology and ecology of sulfate- and sulfur-reducing bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley & Sons, New York, pp 1–2
Willett AI, Rittmann BE (2003) Slow complexation kinetics for ferric iron and EDTA complexes make EDTA non-biodegradable. Biodegradation 4(2):105–121
Wingender J, Neu TR, Flemming HC (1999) What are bacterial extracellular polymeric substances. In: Wingender J, Neu TR, Flemming HC (eds) Microbial extracellular polymeric substances: characterization, structure and function, Springer-Verlag Berlin Heidelberg
Yee N, Fein JB (2001) Cd adsorption onto bacterial surfaces: a universal adsorption edge? Geochim Cosmochim Acta 65(13):2037–2042
Yee N, Fein JB (2003) Quantifying metal adsorption onto bacterial mixtures: a test and application of the surface complexation model. Gemicrobiol J 20:43–60
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Schwarz, A.O., Rittmann, B.E. A biogeochemical framework for metal detoxification in sulfidic systems. Biodegradation 18, 675–692 (2007). https://doi.org/10.1007/s10532-007-9101-2
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DOI: https://doi.org/10.1007/s10532-007-9101-2