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Humic Substances and Extracellular Electron Transfer

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Abstract

Humic substances (HS) are redox-active organic molecules that are present in virtually all environments. A wide variety of bacteria including Fe(III)-reducers, sulfate reducers, methanogens, and fermenting bacteria can reduce HS and in a second, abiotic step, the reduced HS can transfer their electrons to terminal electron acceptors such as poorly soluble Fe(III) minerals, in summary a process called humic substance electron shuttling. Electron shuttling between HS-reducing bacteria and Fe(III) minerals can increase the rate of Fe(III) reduction compared to direct Fe(III) reduction and, furthermore, enables the indirect reduction of Fe(III) minerals by some bacterial groups that are not able to reduce the Fe(III) minerals directly. This chapter will first summarize the knowledge about the redox properties of humic substances including a discussion of their redox-active functional groups. We then focus on the mechanism of electron shuttling and evaluate the advantages and disadvantages of electron shuttling versus direct contact Fe(III) mineral reduction. The role of solid-phase humics and other extracellular electron shuttles is discussed as well as the environmental consequences for long-range electron transfer via humic substances. The chapter concludes by illustrating some remaining open questions and by providing suggestions for future research.

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References

  • Aeschbacher M, Sander M, Schwarzenbach RP (2010) Novel electrochemical approach to assess the redox properties of humic substances. Environ Sci Technol 44:87–93

    Article  PubMed  CAS  Google Scholar 

  • Aeschbacher M, Vergari D, Schwarzenbach RP, Sander M (2011) Electrochemical analysis of proton and electron transfer equilibria of the reducible moieties in humic acids. Environ Sci Technol 45:8385–8394

    Article  PubMed  CAS  Google Scholar 

  • Aiken GR, McKnight DM, Wershaw RL, MacCarthy P (1985) Humic substances in soil, sediment and water: geochemistry, isolation and characterization. Wiley, New York

    Google Scholar 

  • Amstaetter K, Borch T, Kappler A (2012) Influence of humic acid imposed changes of ferrihydrite aggregation on microbial Fe(III) reduction. Geochim Cosmochim Acta 85:326–341

    Article  CAS  Google Scholar 

  • Bauer I, Kappler A (2009) Rates and extent of reduction of Fe(III) compounds and O2 by humic substances. Environ Sci Technol 43:4902–4908

    Article  PubMed  CAS  Google Scholar 

  • Bauer M, Heitmann T, Macalady DL, Blodau C (2007) Electron transfer capacities and reaction kinetics of peat dissolved organic matter. Environ Sci Technol 41:139–145

    Article  PubMed  CAS  Google Scholar 

  • Benz M, Schink B, Brune A (1998) Humic acid reduction by Propionibacterium freudenreichii and other fermenting bacteria. Appl Environ Microbiol 64:4507–4512

    PubMed  CAS  Google Scholar 

  • Bird LJ, Bonnefoy V, Newman DK (2011) Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol 19:330–340

    Article  PubMed  CAS  Google Scholar 

  • Blodau C, Bauer M, Regenspurg S, Macalady D (2009) Electron accepting capacity of dissolved organic matter as determined by reaction with metallic zinc. Chem Geol 260:186–195

    Article  CAS  Google Scholar 

  • Cervantes FJ, de Bok FAM, Tuan DD, Stams AJM, Lettinga G, Field JA (2002) Reduction of humic substances by halorespiring, sulphate-reducing and methanogenic microorganisms. Environ Microbiol 4:51–57

    Article  PubMed  CAS  Google Scholar 

  • Chen J, Gu BH, Royer RA, Burgos WD (2003) The roles of natural organic matter in chemical and microbial reduction of ferric iron. Sci Total Environ 307:167–178

    Article  PubMed  CAS  Google Scholar 

  • Clarke TA, Edwards MJ, Gates AJ, Hall A, White GF, Bradley J, Reardon CL, Shi L, Beliaev AS, Marshall MJ, Wang Z, Watmough NJ, Fredrickson JK, Zachara JM, Butt JN, Richardson DJ (2011) Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci 108:9384–9389

    Article  PubMed  CAS  Google Scholar 

  • Coates JD, Ellis DJ, Blunt-Harris EL, Gaw CV, Roden EE, Lovley DR (1998) Recovery of humic-reducing bacteria from a diversity of environments. Appl Environ Microbiol 64:1504–1509

    PubMed  CAS  Google Scholar 

  • Dunnivant FM, Schwarzenbach RP, Macalady DL (1992) Reduction of substituted nitrobenzenes in aqueous solutions containing natural organic matter. Environ Sci Technol 26:2133–2141

    Article  CAS  Google Scholar 

  • Einsiedl F, Mayer B, Schafer T (2008) Evidence for incorporation of H2S in groundwater fulvic acids from stable isotope ratios and sulfur K-edge X-ray absorption near edge structure spectroscopy. Environ Sci Technol 42:2439–2444

    Article  PubMed  CAS  Google Scholar 

  • Emmerich M, Kappler A (2012) Absence of humic substance reduction by the acidophilic Fe(III)-reducing strain Acidiphilium SJH: implications for its Fe(III) reduction mechanism and for the stimulation of natural organohalogen formation. Biogeochemistry 109:219–231

    Article  CAS  Google Scholar 

  • Fimmen RL, Cory RM, Chin YP, Trouts TD, McKnight DM (2007) Probing the oxidation-reduction properties of terrestrially and microbially derived dissolved organic matter. Geochim Cosmochim Acta 71:3003–3015

    Article  CAS  Google Scholar 

  • Gescher JS, Cordova CD, Spormann AM (2008) Dissimilatory iron reduction in Escherichia coli: identification of cymA of Shewanella oneidensis and napC of E-coli as ferric reductases. Mol Microbiol 68:706–719

    Article  PubMed  CAS  Google Scholar 

  • Gray HB, Winkler JR (2005) Long-range electron transfer. Proc Natl Acad Sci U S A 102:3534–3539

    Article  PubMed  CAS  Google Scholar 

  • Hernandez ME, Kappler A, Newman DK (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70:921–928

    Article  PubMed  CAS  Google Scholar 

  • Jiang J, Kappler A (2008) Kinetics of microbial and chemical reduction of humic substances: implications for electron shuttling. Environ Sci Technol 42:3563–3569

    Article  PubMed  CAS  Google Scholar 

  • Jiang J, Bauer I, Paul A, Kappler A (2009) Arsenic redox changes by microbially and chemically formed semiquinone radicals and hydroquinones in a humic substance model quinone. Environ Sci Technol 43:3639–3645

    Article  PubMed  CAS  Google Scholar 

  • Kappler A, Haderlein SB (2003) Natural organic matter as reductant for chlorinated aliphatic pollutants. Environ Sci Technol 37:2714–2719

    Article  PubMed  CAS  Google Scholar 

  • Kappler A, Straub KL (2005) Geomicrobiological cycling of iron. Rev Mineral Geochem 59:85–108

    Article  CAS  Google Scholar 

  • Kappler A, Benz M, Schink B, Brune A (2004) Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment. FEMS Microbiol Ecol 47:85–92

    Article  PubMed  CAS  Google Scholar 

  • Konhauser KO, Kappler A, Roden EE (2011) Iron in microbial metabolisms. Elements 7:89–93

    Article  CAS  Google Scholar 

  • Kulikova NA, Perminova IV, Badun GA, Chernysheva MG, Koroleva OV, Tsvetkova EA (2010) Uptake of humic substances from different sources by E. coli cells under optimum and salt stress conditions estimated with a use of tritium-labeled humic materials. Appl Environ Microbiol AEM.00905-00910

    Google Scholar 

  • Lies DP, Hernandez ME, Kappler A, Mielke RE, Gralnick JA, Newman DK (2005) Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for biofilms. Appl Environ Microbiol 71:4414–4426

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Zachara JM, Foster NS, Strickland J (2007) Kinetics of reductive dissolution of hematite by bioreduced anthraquinone-2,6-disulfonate. Environ Sci Technol 41:7730–7735

    Article  PubMed  CAS  Google Scholar 

  • Lovley DR, Blunt-Harris EL (1999) Role of humic-bound iron as an electron transfer agent in dissimilatory Fe(III) reduction. Appl Environ Microbiol 65:4252–4254

    PubMed  CAS  Google Scholar 

  • Lovley DR, Woodward JC, Chapelle FH (1994) Stimulated anoxic biodegradation of aromatic-hydrocarbons using Fe(III) ligands. Nature 370:128–131

    Article  PubMed  CAS  Google Scholar 

  • Lovley DR, Coates JD, BluntHarris EL, Phillips EJP, Woodward JC (1996) Humic substances as electron acceptors for microbial respiration. Nature 382:445–448

    Article  CAS  Google Scholar 

  • Lovley DR, Fraga JL, Blunt-Harris EL, Hayes LA, Phillips EJP, Coates JD (1998) Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydroch Hydrob 26:152–157

    Article  CAS  Google Scholar 

  • Lovley DR, Fraga JL, Coates JD, Blunt-Harris EL (1999) Humics as an electron donor for anaerobic respiration. Environ Microbiol 1:89–98

    Article  PubMed  CAS  Google Scholar 

  • Macalady DL, Ranville JF (1998) The chemistry and geochemistry of natural organic matter (NOM). In: Macalady DL (ed) Perspectives in environmental chemistry. Oxford University Press, New York

    Google Scholar 

  • MacDonald LH, Moon HS, Jaffé PR (2011) The role of biomass, electron shuttles, and ferrous iron in the kinetics of Geobacter sulfurreducens-mediated ferrihydrite reduction. Water Res 45:1049–1062

    Article  PubMed  CAS  Google Scholar 

  • Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105:3968–3973

    Article  PubMed  CAS  Google Scholar 

  • Marsili E, Sun J, Bond DR (2010) Voltammetry and growth physiology of Geobacter sulfurreducens biofilms as a function of growth stage and imposed electrode potential. Electroanalysis 22:865–874

    Article  CAS  Google Scholar 

  • Maurer F, Christl I, Kretzschmar R (2010) Reduction and reoxidation of humic acid: influence on spectroscopic properties and proton binding. Environ Sci Technol 44:5787–5792

    Article  PubMed  CAS  Google Scholar 

  • Nevin KP, Lovley DR (2000) Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface sediments. Environ Sci Technol 34:2472–2478

    Article  CAS  Google Scholar 

  • Nielsen LP, Risgaard-Petersen N, Fossing H, Christensen PB, Sayama M (2010) Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463:1071–1074

    Article  PubMed  CAS  Google Scholar 

  • Nurmi JT, Tratnyek PG (2002) Electrochemical properties of natural organic matter (NOM), fractions of NOM, and model biogeochemical electron shuttles. Environ Sci Technol 36:617–624

    Article  PubMed  CAS  Google Scholar 

  • Osterberg R, Shirshova L (1997) Oscillating, nonequilibrium redox properties of humic acids. Geochim Cosmochim Acta 61:4599–4604

    Article  CAS  Google Scholar 

  • Peretyazhko T, Sposito G (2006) Reducing capacity of terrestrial humic acids. Geoderma 137:140–146

    Article  CAS  Google Scholar 

  • Piccolo A (2001) The supramolecular structure of humic substances. Soil Sci 166:810–832

    Article  CAS  Google Scholar 

  • Piepenbrock A, Dippon U, Porsch K, Appel E, Kappler A (2011) Dependence of microbial magnetite formation on humic substance and ferrihydrite concentrations. Geochim Cosmochim Acta 75:6844–6858

    Article  CAS  Google Scholar 

  • Rakshit S, Uchimiya M, Sposito G (2009) Iron(III) bioreduction in soil in the presence of added humic substances. Soil Sci Soc Am J 73:65–71

    Article  CAS  Google Scholar 

  • Ratasuk N, Nanny MA (2007) Characterization and quantification of reversible redox sites in humic substances. Environ Sci Technol 41:7844–7850

    Article  PubMed  CAS  Google Scholar 

  • Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101

    Article  PubMed  CAS  Google Scholar 

  • Roden EE, Kappler A, Bauer I, Jiang J, Paul A, Stoesser R, Konishi H, Xu HF (2010) Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat Geosci 3:417–421

    Article  CAS  Google Scholar 

  • Scott DT, McKnight DM, Blunt-Harris EL, Kolesar SE, Lovley DR (1998) Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ Sci Technol 32:2984–2989

    Article  CAS  Google Scholar 

  • Shyu JBH, Lies DP, Newman DK (2002) Protective role of tolC in efflux of the electron shuttle anthraquinone-2,6-disulfonate. J Bacteriol 184:1806–1810

    Article  PubMed  CAS  Google Scholar 

  • Snoeyenbos-West OL, Nevin KP, Anderson RT, Lovley DR (2000) Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb Ecol 39:153–167

    Article  PubMed  CAS  Google Scholar 

  • Sposito G (2011) Electron shuttling by natural organic matter: twenty years after. In: Tratnyek PG, Grundl TJ, Haderlein SB (eds) Aquatic redox chemistry. American Chemical Society, Washington

    Google Scholar 

  • Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions. Wiley, New York

    Google Scholar 

  • Straub KL, Schink B (2004) Ferrihydrite-dependent growth of Sulfurospirillum deleyianum through electron transfer via sulfur cycling. Appl Environ Microbiol 70:5744–5749

    Article  PubMed  CAS  Google Scholar 

  • Straub KL, Benz M, Schink B (2001) Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol Ecol 34:181–186

    Article  PubMed  CAS  Google Scholar 

  • Straub KL, Kappler A, Schink B (2005) Enrichment and isolation of ferric-iron- and humic-acid-reducing bacteria. In: Leadbetter JR (ed) Environmental microbiology. Elsevier Academic Press Inc, San Diego

    Google Scholar 

  • Struyk Z, Sposito G (2001) Redox properties of standard humic acids. Geoderma 102:329–346

    Article  CAS  Google Scholar 

  • Sutton R, Sposito G (2005) Molecular structure in soil humic substances: the new view. Environ Sci Technol 39:9009–9015

    Article  PubMed  CAS  Google Scholar 

  • Uchimiya M, Stone AT (2009) Reversible redox chemistry of quinones: impact on biogeochemical cycles. Chemosphere 77:451–458

    Article  PubMed  CAS  Google Scholar 

  • Visser SA (1964) Oxidation-reduction potentials and capillary activities of humic acids. Nature 204:581

    Google Scholar 

  • von Canstein H, Ogawa J, Shimizu S, Lloyd JR (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74:615–623

    Article  Google Scholar 

  • Voordeckers JW, Kim BC, Izallalen M, Lovley DR (2010) Role of Geobacter sulfurreducens outer surface c-type cytochromes in reduction of soil humic acid and anthraquinone-2,6-disulfonate. Appl Environ Microbiol 76:2371–2375

    Article  PubMed  CAS  Google Scholar 

  • Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764

    Article  PubMed  CAS  Google Scholar 

  • Wolf M, Kappler A, Jiang J, Meckenstock RU (2009) Effects of humic substances and quinones at low concentrations on ferrihydrite reduction by Geobacter metallireducens. Environ Sci Technol 43:5679–5685

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank Prof. Donald Macalady and Dr. Michael Sander for helpful comments on the manuscript. This work was funded by the research group FOR 580 of the German Research Foundation (DFG).

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Correspondence to Andreas Kappler .

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Piepenbrock, A., Kappler, A. (2013). Humic Substances and Extracellular Electron Transfer. In: Gescher, J., Kappler, A. (eds) Microbial Metal Respiration. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-32867-1_5

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