Electron transfer from Shewanella algae BrY to hydrous ferric oxide is mediated by cell-associated melanin
Corresponding Author
Charles E Turick
Department of Microbiology, University of New Hampshire, Durham, NH 03824-2617, USA
*Corresponding author. Present address: Westinghouse Savannah River Co., Environmental Biotechnology Section, Building 999W, Aiken, SC 29808, USA. Tel.: +1 (803) 819-8407; Fax: +1 (803) 819-8432, E-mail address: [email protected]Search for more papers by this authorF Caccavo Jr.
Department of Microbiology, University of New Hampshire, Durham, NH 03824-2617, USA
Department of Biology, Whitworth College, Spokane, WA 99251, USA.
Search for more papers by this authorLouis S Tisa
Department of Microbiology, University of New Hampshire, Durham, NH 03824-2617, USA
Search for more papers by this authorCorresponding Author
Charles E Turick
Department of Microbiology, University of New Hampshire, Durham, NH 03824-2617, USA
*Corresponding author. Present address: Westinghouse Savannah River Co., Environmental Biotechnology Section, Building 999W, Aiken, SC 29808, USA. Tel.: +1 (803) 819-8407; Fax: +1 (803) 819-8432, E-mail address: [email protected]Search for more papers by this authorF Caccavo Jr.
Department of Microbiology, University of New Hampshire, Durham, NH 03824-2617, USA
Department of Biology, Whitworth College, Spokane, WA 99251, USA.
Search for more papers by this authorLouis S Tisa
Department of Microbiology, University of New Hampshire, Durham, NH 03824-2617, USA
Search for more papers by this authorAbstract
Shewanella algae BrY uses insoluble mineral oxides as terminal electron acceptors, but the mechanism of electron transfer from cell surface to mineral surface is not well understood. We tested the hypothesis that cell-associated melanin produced by S. algae BrY serves as an electron conduit for bacterial–mineral reduction. Results from Fourier transform infrared spectroscopy and cell surface hydrophobicity assays indicated that extracellular melanin was associated with the cell surface. With H2 as electron donor, washed cell suspensions of melanin-coated S. algae BrY reduced hydrous ferric oxide (HFO) 10 times faster than cells without melanin. The addition of melanin (20 μg ml−1) to these melanin-free cells increased their HFO reduction rate two-fold. These results suggest that cell-associated melanin acts as an electron conduit for iron mineral reduction by S. algae BrY.
References
- [1] Lovley, D.R, Coates, J.D, Blunt-Harris, E.L, Phillips, E.J.P, Woodward, J.C (1996) Humic substances as electron acceptors for microbial respiration. Nature 382, 445–448.
- [2] Coates, J.D, Ellis, D.J, Blunt-Harris, E.L, Gaw, C.V, Roden, E.E, Lovley, D.R (1998) Recovery of humic-reducing bacteria from a diversity of environments. Appl. Environ. Microbiol. 64, 1504–1509.
- [3] Scott, D.T, McKnight, D.M, Blunt-Harris, E.L, Kolesar, S.E, Lovley, D.R (1998) Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ. Sci. Technol. 32, 2984–2989.
- [4] Newman, D.K, Kolter, R (2000) A role for excreted quinones in extracellular electron transfer. Nature 405, 94–97.
- [5] Doong, R.-A, Schink, B (2002) Cysteine-mediated reductive dissolution of poorly crystaline iron(III) oxides by Geobacter sulfurreducens. Environ. Sci. Technol. 36, 2939–2945.
- [6] Turick, C.E, Tisa, L.S, Caccavo, F Jr. (2002) Melanin production and use as a soluble electron shuttle for Fe(III) oxide reduction and as a terminal electron acceptor by Shewanella algae BrY. Appl. Environ. Microbiol. 68, 2436–2444.
- [7] McGinness, J.E (1972) Mobility gaps: A mechanism for band gaps in melanins. Science 177, 896–897.
- [8] McGinness, J, Corry, P, Proctor, P (1974) Amorphous semiconductor switching in melanins. Science 183, 853–855.
- [9] Menter, J.M, Willis, I (1997) Electron transfer and photoprotective properties of melanins in solution. Pigment Cell Res. 10, 214–217.
- [10] Pullman, A, Pullman, B (1961) The band structure of melanins. Biochim. Biophys. Acta 54, 384–385.
- [11] Das, A, Caccavo, F Jr. (2000) Fe(III) oxide reduction by Shewanella alga BrY requires adhesion. Curr. Microbiol. 40, 344–347.
- [12] Lovley, D.R (1994) Microbial reduction of iron, manganese, and other metals. Adv. Agron. 54, 175–231.
- [13] Ehrlich, H.L (1993) Electron transfer from acetate to the surface of MnO2 particles by a marine bacterium. J. Ind. Microbiol. 12, 121–128.
- [14] Fredrickson, J.K, Gorby, Y.A (1996) Environmental processes mediated by iron-reducing bacteria. Curr. Opin. Biotechnol. 7, 287–294.
- [15] Lovley, D.R (1997) Microbial Fe(III) reduction in subsurface environments. FEMS Microbiol. Rev. 20, 305–315.
- [16] Myers, C.R, Meyers, J.M (1992) Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens MR-1. J. Bacteriol. 174, 3429–3438.
- [17] Nyhus, K.J, Wilborn, A.T, Jacobson, E.S (1997) Ferric iron reduction by Crypotococcus neoformans. Infect. Immun. 65, 434–438.
- [18] Scott, D.E. and Martin, J.P. (1990) Synthesis and degradation of natural and synthetic humic material in soil. In: Humic Substances in Soil and Crop Sciences: Selected Readings (MacCarthy, P., Clapp, C.E., Malcolm, R.L. and Bloom, P.R., Eds.), pp. 37–58. Soil Science Society of America, Madison, WI.
- [19] Coon, S.L, Kotob, S, Jarvis, B.B, Wang, S, Fuqua, W.C, Weiner, R.M (1994) Homogentisic acid is the product of MelA, which mediated melanogenesis in the marine bacterium Shewanella colwelliana D. Appl. Environ. Microbiol. 60, 3006–3010.
- [20] Ruzafa, C, Sanchez-Amat, A, Solano, F (1995) Characterization of the melanogenic system in Vibrio cholerae ATCC 14035. Pigment Cell Res. 8, 147–152.
- [21] Ruzafa, C, Solano, F, Sanchez-Amat, A (1994) The protein encoded by the Shewanella colwelliana melA gene is p-hydroxyphenylpyruvate dioxygenase. FEMS Microbiol. Lett. 124, 179–184.
- [22]
Yabuuchi, E,
Omyama, A (1972) Characterization of ‘pyomelanin’-producing strains of Pseudomonas aeruginosa.
Int. J. Syst. Bacteriol.
22, 53–64.
10.1099/00207713-22-2-53 Google Scholar
- [23] Weiner, R.M, Segall, A.M, Colwell, R.R (1985) Characterization of a marine bacterium associated with Crassostrea virginica (the eastern oyster). Appl. Environ. Microbiol. 49, 83–90.
- [24] Caccavo, F Jr. Blakemore, R.P, Lovley, D.R (1992) A hydrogen-oxidizing, Fe(III)-reducing microorganism from the Great Bay estuary, New Hampshire. Appl. Environ. Microbiol. 58, 3211–3216.
- [25] Hobbie, J.E, Daley, R.J, Jasper, S (1977) Use of Nucleopore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33, 1225–1228.
- [26] Paz, M.A, Fluckiger, R.A, Boak, A, Kagan, H.M, Gallop, P.M (1991) Specific detection of quinoproteins by redox-cycling staining. J. Biol. Chem. 266, 689–692.
- [27] Abu, G.O, Weiner, R.M, Rice, J, Colwell, R.R (1991) Properties of an extracellular adhesive polymer from the marine bacterium, Shewanella colwelliana. Biofouling 3, 69–84.
- [28] Rosenberg, M, Gutnick, D, Rosenberg, E (1980) Adherence of bacteria to hydrocarbons: A simple method for measuring cell-surface hydrophobicity. FEMS Microbiol. Lett. 9, 29–33.
- [29] Ellis, D.H, Griffiths, D.A (1974) The location and analysis of melanins in cell walls of some soil fungi. Can. J. Microbiol. 20, 1379–1386.
- [30] van der Mei, H.C, Noordmans, J, Busscher, H (1989) Molecular surface characterization of oral streptococci by Fourier transform infrared spectroscopy. Biochim. Biophys. Acta 991, 395–401.
- [31] MacCarthy, P. and Rice, J.A. (1985) Spectroscopic methods (other than NMR) for determining functionality in humic substances. In: Humic Substances in Soil, Sediment, and Water (Aiken, G.R., McKnight, D.M., Wershaw, R.L. and MacCarthy, P., Eds.), pp. 527–560. Wiley-Interscience, New York, NY.
- [32] Conley, R.T. (1966) Quantitative analysis. In: Infrared Spectroscopy, pp. 87–175. Allyn and Bacon, Boston, MA.
- [33] Prota, G. (1992) Natural and synthetic melanins. In: Melanins and Melanogenesis (Prota, G., Ed.), pp. 63–87. Academic Press, San Diego, CA.
- [34] White, L.P (1958) Melanin: A naturally occurring cation exchange material. Nature 182, 1427–1428.
- [35] Sakai, D.K (1986) Electrostatic mechanisms of survival of virulent Aeromonas salmonicida strains in river water. Appl. Environ. Microbiol. 51, 1342–1349.
- [36] Obuekwe, C.O, Westlake, D.S.W (1982) Effects of medium composition on cell pigmentation, cytochrome content, and ferric iron reduction in a Pseudomonas sp. isolated from crude oil. Can. J. Microbiol. 28, 989–992.
- [37] Caccavo, F Jr. Schamberger, P.C, Keiding, K, Nielsen, P.H (1997) Role of hydrophobicity in adhesion of the dissimilatory Fe(III)-reducing bacterium Shewanella alga to amorphous Fe(III) oxide. Appl. Environ. Microbiol. 63, 3837–3843.
- [38] Nevin, K.P, Lovley, D.R (2000) Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface environments. Environ. Sci. Technol. 34, 2472–2478.
- [39] Coyne, V.E, Al-Harthi, L (1992) Induction of melanin biosynthesis in Vibrio cholerae. Appl. Environ. Microbiol. 58, 2861–2865.