Rational engineering of Geobacter sulfurreducens electron transfer components: A foundation for building improved Geobacter-based bioelectrochemical technologies

Frontiers in Microbiology

Volumn 6, Issue JUL, 2015, Pages

  Dantas, Joana M ^a   Morgado, Leonor ^a,e   Aklujkar, Muktak ^b   Bruix, Marta ^c   Londer, Yuri Y ^d   Schiffer, Marianne ^d   Raj Pokkuluri, P ^d   Salgueiro, Carlos A ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b TOWSON UNIVERSITY   (United States)

^c INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^d ARGONNE NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Cytochrome c; Extracellular electron transfer; Geobacter; Geobacter mutant strains; Multiheme

Indexed keywords

BIOENGINEERING; CARBON NUCLEAR MAGNETIC RESONANCE; ELECTROCHEMICAL ANALYSIS; ELECTRON TRANSPORT; GENE MUTATION; GEOBACTER SULFURREDUCENS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SIGNAL TRANSDUCTION; THERMODYNAMICS;

GEOBACTER; GEOBACTER SULFURREDUCENS;

EID: 84938847096     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00752     Document Type: Review

References (55)

1. Dantas, J. M., Kokhan, O., Pokkuluri, P. R., and Salgueiro, C. A. (2015a). Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances. Biochim. Biophys. Acta 1847, 1129-1138. doi: 10.1016/j.bbabio.2015.06.004
2. Dantas, J. M., Morgado, L., Catarino, T., Kokhan, O., Raj Pokkuluri, P., and Salgueiro, C. A. (2014). Evidence for interaction between the triheme cytochrome PpcA from Geobacter sulfurreducens and anthrahydroquinone-2,6-disulfonate, an analog of the redox active components of humic substances. Biochim. Biophys. Acta 1837, 750-760. doi: 10.1016/j.bbabio.2014.02.004
3. Dantas, J. M., Morgado, L., Londer, Y. Y., Fernandes, A. P., Louro, R. O., Pokkuluri, P. R., et al. (2012). Pivotal role of the strictly conserved aromatic residue F15 in the cytochrome c7 family. J. Biol. Inorg. Chem. 17, 11-24. doi: 10.1007/s00775-011-0821-8
4. Dantas, J. M., Morgado, L., Pokkuluri, P. R., Turner, D. L., and Salgueiro, C. A. (2013). Solution structure of a mutant of the triheme cytochrome PpcA from Geobacter sulfurreducens sheds light on the role of the conserved aromatic residue F15. Biochim. Biophys. Acta 1827, 484-492. doi: 10.1016/j.bbabio.2012.12.008
5. Dantas, J. M., Salgueiro, C. A., and Bruix, M. (2015b). Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcD from Geobacter sulfurreducens. Biomol. NMR Assign. 9, 211-214. doi: 10.1007/s12104-014-9576-9
6. Dantas, J. M., Saraiva, I. H., Morgado, L., Silva, M. A., Schiffer, M., Salgueiro, C. A., et al. (2011). Orientation of the axial ligands and magnetic properties of the hemes in the cytochrome c7 family from Geobacter sulfurreducens determined by paramagnetic NMR. Dalton Trans. 40, 12713-12718. doi: 10.1039/c1dt10975h
7. Ding, Y. H., Hixson, K. K., Aklujkar, M. A., Lipton, M. S., Smith, R. D., Lovley, D. R., et al. (2008). Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor. Biochim. Biophys. Acta 1784, 1935-1941. doi: 10.1016/j.bbapap.2008.06.011
8. Ding, Y. H., Hixson, K. K., Giometti, C. S., Stanley, A., Esteve-Núñez, A., Khare, T., et al. (2006). The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions. Biochim. Biophys. Acta 1764, 1198-1206. doi: 10.1016/j.bbapap.2006.04.017
9. Esteve-Núñez, A., Sosnik, J., Visconti, P., and Lovley, D. R. (2008). Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens. Environ. Microbiol. 10, 497-505. doi: 10.1111/j.1462-2920.2007.01470.x
10. Fernandes, A. P., Couto, I., Morgado, L., Londer, Y. Y., and Salgueiro, C. A. (2008). Isotopic labeling of c-type multiheme cytochromes overexpressed in E. coli. Protein Expr. Purif. 59, 182-188. doi: 10.1016/j.pep.2008.02.001
11. Fonseca, B. M., Paquete, C. M., Salgueiro, C. A., and Louro, R. O. (2012a). The role of intramolecular interactions in the functional control of multiheme cytochromes c. FEBS Lett. 586, 504-509. doi: 10.1016/j.febslet.2011.08.019
12. Fonseca, B. M., Tien, M., Rivera, M., Shi, L., and Louro, R. O. (2012b). Efficient and selective isotopic labeling of hemes to facilitate the study of multiheme proteins. Biotechniques 1-7. doi: 10.2144/000113859
13. Holmes, D. E., Chaudhuri, S. K., Nevin, K. P., Mehta, T., Methé, B. A., Liu, A., et al. (2006). Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ. Microbiol. 8, 1805-1815. doi: 10.1111/j.1462-2920.2006.01065.x
14. Kim, B. C., Leang, C., Ding, Y. H., Glaven, R. H., Coppi, M. V., and Lovley, D. R. (2005). OmcF, a putative c-type monoheme outer membrane cytochrome required for the expression of other outer membrane cytochromes in Geobacter sulfurreducens. J. Bacteriol. 187, 4505-4513. doi: 10.1128/JB.187.13.4505-4513.2005
15. Kim, B. C., and Lovley, D. R. (2008). Investigation of direct vs. indirect involvement of the c-type cytochrome MacA in Fe(III) reduction by Geobacter sulfurreducens. FEMS Microbiol. Lett. 286, 39-44. doi: 10.1111/j.1574-6968.2008.01252.x
16. Kim, B. C., Postier, B. L., Didonato, R. J., Chaudhuri, S. K., Nevin, K. P., and Lovley, D. R. (2008). Insights into genes involved in electricity generation in Geobacter sulfurreducens via whole genome microarray analysis of the OmcF-deficient mutant. Bioelectrochemistry 73, 70-75. doi: 10.1016/j.bioelechem.2008.04.023
17. Leang, C., Coppi, M. V., and Lovley, D. R. (2003). OmcB, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 185, 2096-2103. doi: 10.1128/JB.185.7.2096-2103.2003
18. Levar, C. E., Chan, C. H., Mehta-Kolte, M. G., and Bond, D. R. (2014). An inner membrane cytochrome required only for reduction of high redox potential extracellular electron acceptors. MBio 5, e02034. doi: 10.1128/mBio.02034-14
19. Liu, Y., Wang, Z., Liu, J., Levar, C., Edwards, M. J., Babauta, J. T., et al. (2014). A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA. Environ. Microbiol. Rep. 6, 776-785. doi: 10.1111/1758-2229.12204
20. Lloyd, J. R., Leang, C., Hodges Myerson, A. L., Coppi, M. V., Ciufo, S., Methe, B., et al. (2003). Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochem. J. 369, 153-161. doi: 10.1042/BJ20020597
21. Londer, Y. Y., Pokkuluri, P. R., Erickson, J., Orshonsky, V., and Schiffer, M. (2005). Heterologous expression of hexaheme fragments of a multidomain cytochrome from Geobacter sulfurreducens representing a novel class of cytochromes c. Protein Expr. Purif. 39, 254-260. doi: 10.1016/j.pep.2004.10.015
22. Londer, Y. Y., Pokkuluri, P. R., Orshonsky, V., Orshonsky, L., and Schiffer, M. (2006). Heterologous expression of dodecaheme "nanowire" cytochromes c from Geobacter sulfurreducens. Protein Expr. Purif. 47, 241-248. doi: 10.1016/j.pep.2005.11.017
23. Londer, Y. Y., Pokkuluri, P. R., Tiede, D. M., and Schiffer, M. (2002). Production and preliminary characterization of a recombinant triheme cytochrome c7 from Geobacter sulfurreducens in Escherichia coli. Biochim. Biophys. Acta 1554, 202-211. doi: 10.1016/S0005-2728(02)00244-X
24. Lovley, D. R., Philips, E. J. P., Gorby, Y. A., and Landa, E. R. (1991). Microbial reduction of uranium. Nature 350, 413-416. doi: 10.1038/350413a0
25. Lovley, D. R., and Phillips, E. J. (1988). Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54, 1472-1480.
26. Lovley, D. R., Stolz, J. F., Nord, G. L. Jr., and Philips, E. J. P. (1987). Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 330, 252-254. doi: 10.1038/330252a0
27. Mehta, T., Coppi, M. V., Childers, S. E., and Lovley, D. R. (2005). Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71, 8634-8641. doi: 10.1128/AEM.71.12.8634-8641.2005
28. Methé, B. A., Nelson, K. E., Eisen, J. A., Paulsen, I. T., Nelson, W., Heidelberg, J. F., et al. (2003). Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302, 1967-1969. doi: 10.1126/science.1088727
29. Morgado, L., Bruix, M., Londer, Y. Y., Pokkuluri, P. R., Schiffer, M., and Salgueiro, C. A. (2007). Redox-linked conformational changes of a multiheme cytochrome from Geobacter sulfurreducens. Biochem. Biophys. Res. Commun. 360, 194-198. doi: 10.1016/j.bbrc.2007.06.026
30. Morgado, L., Bruix, M., Orshonsky, V., Londer, Y. Y., Duke, N. E., Yang, X., et al. (2008). Structural insights into the modulation of the redox properties of two Geobacter sulfurreducens homologous triheme cytochromes. Biochim. Biophys. Acta 1777, 1157-1165. doi: 10.1016/j.bbabio.2008.04.043
31. Morgado, L., Bruix, M., Pessanha, M., Londer, Y. Y., and Salgueiro, C. A. (2010a). Thermodynamic characterization of a triheme cytochrome family from Geobacter sulfurreducens reveals mechanistic and functional diversity. Biophys. J. 99, 293-301. doi: 10.1016/j.bpj.2010.04.017
32. Morgado, L., Dantas, J. M., Bruix, M., Londer, Y. Y., and Salgueiro, C. A. (2012a). Fine tuning of redox networks on multiheme cytochromes from Geobacter sulfurreducens drives physiological electron/proton energy transduction. Bioinorg. Chem. Appl. 2012, 1-9. doi: 10.1155/2012/298739
33. Morgado, L., Dantas, J. M., Simoes, T., Londer, Y. Y., Pokkuluri, P. R., and Salgueiro, C. A. (2013). Role of Met(58) in the regulation of electron/proton transfer in trihaem cytochrome PpcA from Geobacter sulfurreducens. Biosci. Rep. 33, 11-22. doi: 10.1042/BSR20120086
34. Morgado, L., Fernandes, A. P., Londer, Y. Y., Bruix, M., and Salgueiro, C. A. (2010b). One simple step in the identification of the cofactors signals, one giant leap for the solution structure determination of multiheme proteins. Biochem. Biophys. Res. Commun. 393, 466-470. doi: 10.1016/j.bbrc.2010.02.024
35. Morgado, L., Lourenço, S., Londer, Y. Y., Schiffer, M., Pokkuluri, P. R., and Salgueiro, C. (2014). Dissecting the functional role of key residues in triheme cytochrome PpcA: a path to rational design of G. sulfurreducens strains with enhanced electron transfer capabilities. PLoS ONE 9:e105566. doi: 10.1371/journal.pone.0105566
36. Morgado, L., Paixão, V. B., Salgueiro, C. A., and Bruix, M. (2011). Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcA from Geobacter sulfurreducens. Biomol. NMR Assign. 5, 113-116. doi: 10.1007/s12104-010-9280-3
37. Morgado, L., Paixão, V. B., Schiffer, M., Pokkuluri, P. R., Bruix, M., and Salgueiro, C. A. (2012b). Revealing the structural origin of the redox-Bohr effect: the first solution structure of a cytochrome from Geobacter sulfurreducens. Biochem. J. 441, 179-187. doi: 10.1042/BJ20111103
38. Morgado, L., Saraiva, I. H., Louro, R. O., and Salgueiro, C. A. (2010c). Orientation of the axial ligands and magnetic properties of the hemes in the triheme ferricytochrome PpcA from G. sulfurreducens determined by paramagnetic NMR. FEBS Lett. 584, 3442-3445. doi: 10.1016/j.febslet.2010.06.043
39. Moss, G. P. (1988). Nomenclature of tetrapyrroles. Recommendations 1986 IUPAC-IUB joint commission on biochemical nomenclature (JCBN). Eur. J. Biochem. 178, 277-328. doi: 10.1111/j.1432-1033.1988.tb14453.x
40. Nevin, K. P., Kim, B. C., Glaven, R. H., Johnson, J. P., Woodard, T. L., Methe, B. A., et al. (2009). Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS ONE 4:e5628. doi: 10.1371/journal.pone.0005628
41. Nevin, K. P., Richter, H., Covalla, S. F., Johnson, J. P., Woodard, T. L., Orloff, A. L., et al. (2008). Power output and columbic efficiencies from biofilms of Geobacter sulfurreducens comparable to mixed community microbial fuel cells. Environ. Microbiol. 10, 2505-2514. doi: 10.1111/j.1462-2920.2008.01675.x
42. Paixão, V. B., Vis, H., and Turner, D. L. (2010). Redox linked conformational changes in cytochrome c3 from Desulfovibrio desulfuricans ATCC 27774. Biochemistry 49, 9620-9629. doi: 10.1021/bi101237w
43. Pessanha, M., Londer, Y. Y., Long, W. C., Erickson, J., Pokkuluri, P. R., Schiffer, M., et al. (2004). Redox characterization of Geobacter sulfurreducens cytochrome c7: physiological relevance of the conserved residue F15 probed by site-specific mutagenesis. Biochemistry 43, 9909-9917. doi: 10.1021/bi0492859
44. Pessanha, M., Morgado, L., Louro, R. O., Londer, Y. Y., Pokkuluri, P. R., Schiffer, M., et al. (2006). Thermodynamic characterization of triheme cytochrome PpcA from Geobacter sulfurreducens: evidence for a role played in e-/H+ energy transduction. Biochemistry 45, 13910-13917. doi: 10.1021/bi061394v
45. Pokkuluri, P. R., Londer, Y. Y., Duke, N. E., Erickson, J., Pessanha, M., Salgueiro, C. A., et al. (2004a). Structure of a novel c7-type three-heme cytochrome domain from a multidomain cytochrome c polymer. Protein. Sci. 13, 1684-1692. doi: 10.1110/ps.04626204
46. Pokkuluri, P. R., Londer, Y. Y., Duke, N. E., Long, W. C., and Schiffer, M. (2004b). Family of cytochrome c7-type proteins from Geobacter sulfurreducens: structure of one cytochrome c7 at 1.45 Å resolution. Biochemistry 43, 849-859. doi: 10.1021/bi0301439
47. Pokkuluri, P. R., Londer, Y. Y., Wood, S. J., Duke, N. E., Morgado, L., Salgueiro, C. A., et al. (2009). Outer membrane cytochrome c, OmcF, from Geobacter sulfurreducens: high structural similarity to an algal cytochrome c6. Proteins 74, 266-270. doi: 10.1002/prot.22260
48. Pokkuluri, P. R., Londer, Y. Y., Yang, X., Duke, N. E., Erickson, J., Orshonsky, V., et al. (2010). Structural characterization of a family of cytochromes c7 involved in Fe(III) respiration by Geobacter sulfurreducens. Biochim. Biophys. Acta 1797, 222-232. doi: 10.1016/j.bbabio.2009.10.007
49. Shelobolina, E. S., Coppi, M. V., Korenevsky, A. A., Didonato, L. N., Sullivan, S. A., Konishi, H., et al. (2007). Importance of c-type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BMC Microbiol. 7:16. doi: 10.1186/1471-2180-7-16
50. Shi, L., Lin, J. T., Markillie, L. M., Squier, T. C., and Hooker, B. S. (2005). Overexpression of multi-heme c-type cytochromes. Biotechniques 38, 297-299. doi: 10.2144/05382PT01
51. Smith, J. A., Tremblay, P. L., Shrestha, P. M., Snoeyenbos-West, O. L., Franks, A. E., Nevin, K. P., et al. (2014). Going wireless: Fe(III) oxide reduction without pili by Geobacter sulfurreducens strain JS-1. Appl. Environ. Microbiol. 80, 4331-4340. doi: 10.1128/AEM.01122-14
52. Turner, D. L., Salgueiro, C. A., Catarino, T., Legall, J., and Xavier, A. V. (1996). NMR studies of cooperativity in the tetrahaem cytochrome c3 from Desulfovibrio vulgaris. Eur. J. Biochem. 241, 723-731. doi: 10.1111/j.1432-1033.1996.00723.x
53. Voordeckers, J. W., Kim, B. C., Izallalen, M., and Lovley, D. R. (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. doi: 10.1128/AEM.02250-09
54. Wl, D. (2002). The PyMOL Molecular Graphics System. Available online at: http://www.pymol.org
55. Yi, H., Nevin, K. P., Kim, B. C., Franks, A. E., Klimes, A., Tender, L. M., et al. (2009). Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens. Bioelectron. 24, 3498-3503. doi: 10.1016/j.bios.2009.05.004