Genomic analyses of bacterial porin-cytochrome gene clusters

Frontiers in Microbiology

Volumn 5, Issue NOV, 2014, Pages

  Shi, Liang ^a   Fredrickson, James K ^a   Zachara, John M ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

C type cytochromes with multiple hemes; Extracellular electron transfer; Metal reduction; Outer membrane; Porin cytochrome protein complex

Indexed keywords

CYTOCHROME; FERRIC ION; FORMATE DEHYDROGENASE; HEME; MANGANESE OXIDE; PORIN; QUINONE DERIVATIVE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; BIOGEOCHEMICAL CYCLING; ELECTRON TRANSPORT; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC CODE; GENETIC TRANSCRIPTION; GEOBACTER SULFURREDUCENS; MICROBIAL GENOME; NONHUMAN; PHYLOGENY;

EID: 84987815000     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00657     Document Type: Article

References (63)

1. Aklujkar, M., Coppi, M. V., Leang, C., Kim, B. C., Chavan, M. A., Perpetua, L. A., et al. (2013). Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens. Microbiology 159, 515-535. doi: 10.1099/mic.0.064089-0
2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2
3. Bagos, P. G., Liakopoulos, T. D., Spyropoulos, I. C., and Hamodrakas, S. J. (2004a). PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins. Nucleic Acids Res. 32, W400-W404. doi: 10.1093/nar/gkh417
4. Bagos, P. G., Liakopoulos, T. D., Spyropoulos, I. C., and Hamodrakas, S. J. (2004b). A Hidden Markov Model method, capable of predicting and discriminating beta-barrel outer membrane proteins. BMC Bioinformatics 5:29. doi: 10.1186/1471-2105-5-29
5. Belchik, S. M., Kennedy, D. W., Dohnalkova, A. C., Wang, Y., Sevinc, P. C., Wu, H., et al. (2011). Extracellular reduction of hexavalant chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 77, 4035-4041. doi: 10.1128/AEM.02463-10
6. Bird, L. J., Bonnefoy, V., and Newman, D. K. (2011). Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol. 19, 330-340. doi: 10.1016/j.tim.2011.05.001
7. Butler, J. E., Young, N. D., and Lovley, D. R. (2010). Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 11:40. doi: 10.1186/1471-2164-11-40
8. Clarke, T. A., Edwards, M. J., Gates, A. J., Hall, A., White, G. F., Bradley, J., et al. (2011). Structure of a bacterial cell surface decaheme electron conduit. Proc. Natl. Acad. Sci. U.S.A. 108, 9384-9389. doi: 10.1073/pnas.1017200108
9. Cologgi, D. L., Lampa-Pastirk, S., Speers, A. M., Kelly, S. D., and Reguera, G. (2011). Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc. Natl. Acad. Sci. U.S.A. 108, 15248-15252. doi: 10.1073/pnas.1108616108
10. Coursolle, D., and Gralnick, J. A. (2010). Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol. Microbiol. 77, 995-1008. doi: 10.1111/j.1365-2958.2010.07266.x
11. Edwards, M. J., Baiden, N. A., Johs, A., Tomanicek, S. J., Liang, L., Shi, L., et al. (2014). The X-ray crystal structure of Shewanella oneidensis OmcA reveals new insight at the microbe-mineral interface. FEBS Lett. 588, 1886-1890. doi: 10.1016/j.febslet.2014.04.013
12. Edwards, M. J., Hall, A., Shi, L., Fredrickson, J. K., Zachara, J. M., Butt, J. N., et al. (2012). The crystal structure of the extracellular 11-heme cytochrome UndA reveals a conserved 10-heme motif and defined binding site for soluble iron chelates. Structure 20, 1275-1284. doi: 10.1016/j.str.2012.04.016
13. Emerson, D., Field, E. K., Chertkov, O., Davenport, K. W., Goodwin, L., Munk, C., et al. (2013). Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics. Front. Microbiol. 4:254. doi: 10.3389/fmicb.2013.00254
14. Firer-Sherwood, M. A., Ando, N., Drennan, C. L., and Elliott, S. J. (2011). Solution-based structural analysis of the decaheme cytochrome, MtrA, by small angle X-ray scattering and analytical ultracentrifugation. J. Phys. Chem. B 115, 11208-11214. doi: 10.1021/jp203603r
15. Fredrickson, J. K., Romine, M. F., Beliaev, A. S., Auchtung, J. M., Driscoll, M. E., Gardner, T. S., et al. (2008). Towards environmental systems biology of Shewanella. Nat. Rev. Microbiol. 6, 592-603. doi: 10.1038/nrmicro1947
16. Giovannelli, D., Ricci, J., Perez-Rodriguez, I., Hugler, M., O'Brien, C., Keddis, R., et al. (2012). Complete genome sequence of Thermovibrio ammonificans HB-1(T), a thermophilic, chemolithoautotrophic bacterium isolated from a deep-sea hydrothermal vent. Stand. Genomic Sci. 7, 82-90. doi: 10.4056/sigs.2856770
17. Gralnick, J. A., Vali, H., Lies, D. P., and Newman, D. K. (2006). Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc. Natl. Acad. Sci. U.S.A. 103, 4669-4674. doi: 10.1073/pnas.0505959103
18. Gross, R., Pisa, R., Sanger, M., Lancaster, C. R., and Simon, J. (2004). Characterization of the menaquinone reduction site in the diheme cytochrome b membrane anchor of Wolinella succinogenes NiFe-hydrogenase. J. Biol. Chem. 279, 274-281. doi: 10.1074/jbc.M310610200
19. Hartshorne, R. S., Jepson, B. N., Clarke, T. A., Field, S. J., Fredrickson, J., Zachara, J., et al. (2007). Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors. J. Biol. Inorg. Chem. 12, 1083-1094. doi: 10.1007/s00775-007-0278-y
20. Hartshorne, R. S., Reardon, C. L., Ross, D., Nuester, J., Clarke, T. A., Gates, A. J., et al. (2009). Characterization of an electron conduit between bacteria and the extracellular environment. Proc. Natl. Acad. Sci. U.S.A. 106, 22169-22174. doi: 10.1073/pnas.0900086106
21. Iino, T., Mori, K., Uchino, Y., Nakagawa, T., Harayama, S., and Suzuki, K. (2010). Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria. Int. J. Syst. Evol. Microbiol. 60, 1376-1382. doi: 10.1099/ijs.0.012484-0
22. Inoue, K., Qian, X., Morgado, L., Kim, B. C., Mester, T., Izallalen, M., et al. (2010). Purification and characterization of OmcZ, an outer-surface, octaheme c-type cytochrome essential for optimal current production by Geobacter sulfurreducens. Appl. Environ. Microbiol. 76, 3999-4007. doi: 10.1128/AEM.00027-10
23. Jiao, Y., and Newman, D. K. (2007). The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J. Bacteriol. 189, 1765-1773. doi: 10.1128/JB.00776-06
24. Juncker, A. S., Willenbrock, H., Von Heijne, G., Brunak, S., Nielsen, H., and Krogh, A. (2003). Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12, 1652-1662. doi: 10.1110/ps.0303703
25. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580. doi: 10.1006/jmbi.2000.4315
26. 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
27. Leang, C., and Lovley, D. R. (2005). Regulation of two highly similar genes, omcB and omcC, in a 10 kb chromosomal duplication in Geobacter sulfurreducens. Microbiology 151, 1761-1767. doi: 10.1099/mic.0.27870-0
28. L'Haridon, S., Cilia, V., Messner, P., Raguenes, G., Gambacorta, A., Sleytr, U. B., et al. (1998). Desulfurobacterium thermolithotrophum gen. nov., sp. nov., a novel autotrophic, sulphur-reducing bacterium isolated from a deep-sea hydrothermal vent. Int. J. Syst. Bacteriol. 48(Pt 3), 701-711. doi: 10.1099/00207713-48-3-701
29. Liu, J., Pearce, C. I., Liu, C., Wang, Z., Shi, L., Arenholz, E., et al. (2013). Fe(3-x)Ti(x)O4 nanoparticles as tunable probes of microbial metal oxidation. J. Am. Chem. Soc. 135, 8896-8907. doi: 10.1021/ja4015343
30. Liu, J., Wang, Z., Belchik, S. M., Edwards, M. J., Liu, C., Kennedy, D. W., et al. (2012). Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front. Microbiol. 3:37. doi: 10.3389/fmicb.2012.00037
31. 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. doi: 10.1111/1758-2229.12204. [Epub ahead of print].
32. Lovley, D. R. (2006). Bug juice: harvesting electricity with microorganisms. Nat. Rev. Microbiol. 4, 497-508. doi: 10.1038/nrmicro1442
33. Lovley, D. R. (2012). Electromicrobiology. Annu. Rev. Microbiol. 66, 391-409. doi: 10.1146/annurev-micro-092611-150104
34. Lovley, D. R., Holmes, D. E., and Nevin, K. P. (2004). Dissimilatory Fe(III) and Mn(IV) reduction. Adv. Microb. Physiol. 49, 219-286. doi: 10.1016/S0065-2911(04)49005-5
35. Lovley, D. R., Ueki, T., Zhang, T., Malvankar, N. S., Shrestha, P. M., Flanagan, K. A., et al. (2011). Geobacter: the microbe electric's physiology, ecology, and practical applications. Adv. Microb. Physiol. 59, 1-100. doi: 10.1016/B978-0-12-387661-4.00004-5
36. Lower, B. H., Yongsunthon, R., Shi, L., Wildling, L., Gruber, H. J., Wigginton, N. S., et al. (2009). Antibody recognition force microscopy shows that outer membrane cytochromes OmcA and MtrC are expressed on the exterior surface of Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 75, 2931-2935. doi: 10.1128/AEM.02108-08
37. Marritt, S. J., Lowe, T. G., Bye, J., McMillan, D. G., Shi, L., Fredrickson, J., et al. (2012a). A functional description of CymA, an electron-transfer hub supporting anaerobic respiratory flexibility in Shewanella. Biochem. J. 444, 465-474. doi: 10.1042/BJ20120197
38. Marritt, S. J., McMillan, D. G., Shi, L., Fredrickson, J. K., Zachara, J. M., Richardson, D. J., et al. (2012b). The roles of CymA in support of the respiratory flexibility of Shewanella oneidensis MR-1. Biochem. Soc. Trans. 40, 1217-1221. doi: 10.1042/BST20120150
39. McMillan, D. G., Marritt, S. J., Butt, J. N., and Jeuken, L. J. (2012). Menaquinone-7 is specific cofactor in tetraheme quinol dehydrogenase CymA. J. Biol. Chem. 287, 14215-14225. doi: 10.1074/jbc.M112.348813
40. McMillan, D. G., Marritt, S. J., Firer-Sherwood, M. A., Shi, L., Richardson, D. J., Evans, S. D., et al. (2013). Protein-protein interaction regulates the direction of catalysis and electron transfer in a redox enzyme complex. J. Am. Chem. Soc. 135, 10550-10556. doi: 10.1021/ja405072z
41. Myhr, S., and Torsvik, T. (2000). Denitrovibrio acetiphilus, a novel genus and species of dissimilatory nitrate-reducing bacterium isolated from an oil reservoir model column. Int. J. Syst. Evol. Microbiol. 50(Pt 4), 1611-1619. doi: 10.1099/00207713-50-4-1611
42. Narasingarao, P., and Haggblom, M. M. (2007). Identification of anaerobic selenate-respiring bacteria from aquatic sediments. Appl. Environ. Microbiol. 73, 3519-3527. doi: 10.1128/AEM.02737-06
43. Nissen, S., Liu, X., Chourey, K., Hettich, R. L., Wagner, D. D., Pfiffner, S. M., et al. (2012). Comparative c-type cytochrome expression analysis in Shewanella oneidensis strain MR-1 and Anaeromyxobacter dehalogenans strain 2CP-C grown with soluble and insoluble oxidized metal electron acceptors. Biochem. Soc. Trans. 40, 1204-1210. doi: 10.1042/BST20120182
44. Pitts, K. E., Dobbin, P. S., Reyes-Ramirez, F., Thomson, A. J., Richardson, D. J., and Seward, H. E. (2003). Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA: expression in Escherichia coli confers the ability to reduce soluble Fe(III) chelates. J. Biol. Chem. 278, 27758-27765. doi: 10.1074/jbc.M302582200
45. Rauschenbach, I., Narasingarao, P., and Haggblom, M. M. (2011a). Desulfurispirillum indicum sp. nov., a selenate- and selenite-respiring bacterium isolated from an estuarine canal. Int. J. Syst. Evol. Microbiol. 61, 654-658. doi: 10.1099/ijs.0.022392-0
46. Rauschenbach, I., Yee, N., Haggblom, M. M., and Bini, E. (2011b). Energy metabolism and multiple respiratory pathways revealed by genome sequencing of Desulfurispirillum indicum strain S5. Environ. Microbiol. 13, 1611-1621. doi: 10.1111/j.1462-2920.2011.02473.x
47. Reardon, C. L., Dohnalkova, A. C., Nachimuthu, P., Kennedy, D. W., Saffarini, D. A., Arey, B. W., et al. (2010). Role of outer-membrane cytochromes MtrC and OmcA in the biomineralization of ferrihydrite by Shewanella oneidensis MR-1. Geobiology 8, 56-68. doi: 10.1111/j.1472-4669.2009.00226.x
48. Richardson, D. J., Butt, J. N., Fredrickson, J. K., Zachara, J. M., Shi, L., Edwards, M. J., et al. (2012). The "porin-cytochrome" model for microbe-to-mineral electron transfer. Mol. Microbiol. 85, 201-212. doi: 10.1111/j.1365-2958.2012.08088.x
49. Roden, E. E., and Lovley, D. R. (1993). Dissimilatory Fe(III) reduction by the marine microorganism Desulfuromonas acetoxidans. Appl. Environ. Microbiol. 59, 734-742.
50. Shi, L., Belchik, S. M., Wang, Z., Kennedy, D. W., Dohnalkova, A. C., Marshall, M. J., et al. (2011). Identification and characterization of UndAHRCR-6, an outer membrane endecaheme c-type cytochrome of Shewanella sp. strain HRCR-6. Appl. Environ. Microbiol. 77, 5521-5523. doi: 10.1128/AEM.00614-11
51. Shi, L., Chen, B., Wang, Z., Elias, D. A., Mayer, M. U., Gorby, Y. A., et al. (2006). Isolation of a high-affinity functional protein complex between OmcA and MtrC: two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1. J. Bacteriol. 188, 4705-4714. doi: 10.1128/JB.01966-05
52. 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
53. Shi, L., Richardson, D. J., Wang, Z., Kerisit, S. N., Rosso, K. M., Zachara, J. M., et al. (2009). The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ. Microbiol. Rep. 1, 220-227. doi: 10.1111/j.1758-2229.2009.00035.x
54. Shi, L., Rosso, K. M., Clarke, T. A., Richardson, D. J., Zachara, J. M., and Fredrickson, J. K. (2012a). Molecular underpinnings of Fe(III) oxide reduction by Shewanella Oneidensis MR-1. Front. Microbiol. 3:50. doi: 10.3389/fmicb.2012.00050
55. Shi, L., Rosso, K. M., Zachara, J. M., and Fredrickson, J. K. (2012b). Mtr extracellular electron-transfer pathways in Fe(III)-reducing or Fe(II)-oxidizing bacteria: a genomic perspective. Biochem. Soc. Trans. 40, 1261-1267. doi: 10.1042/BST20120098
56. Shi, L., Squier, T. C., Zachara, J. M., and Fredrickson, J. K. (2007). Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol. Microbiol. 65, 12-20. doi: 10.1111/j.1365-2958.2007.05783.x
57. Sorokin, D. Y., Tourova, T. P., Mussmann, M., and Muyzer, G. (2008). Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: two novel representatives of reductive sulfur cycle from soda lakes. Extremophiles 12, 431-439. doi: 10.1007/s00792-008-0148-8
58. Speth, D. R., Hu, B., Bosch, N., Keltjens, J. T., Stunnenberg, H. G., and Jetten, M. S. (2012). Comparative genomics of two independently enriched "candidatus Kuenenia stuttgartiensis" anammox bacteria. Front. Microbiol. 3:307. doi: 10.3389/fmicb.2012.00307
59. Stevens, J. M., Daltrop, O., Allen, J. W., and Ferguson, S. J. (2004). C-type cytochrome formation: chemical and biological enigmas. Acc. Chem. Res. 37, 999-1007. doi: 10.1021/ar030266l
60. Summers, Z. M., Fogarty, H. E., Leang, C., Franks, A. E., Malvankar, N. S., and Lovley, D. R. (2010). Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330, 1413-1415. doi: 10.1126/science.1196526
61. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
62. Weber, K. A., Achenbach, L. A., and Coates, J. D. (2006). Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat. Rev. Microbiol. 4, 752-764. doi: 10.1038/nrmicro1490
63. White, G. F., Shi, Z., Shi, L., Wang, Z., Dohnalkova, A. C., Marshall, M. J., et al. (2013). Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals. Proc. Natl. Acad. Sci. U.S.A. 110, 6346-6351. doi: 10.1073/pnas.1220074110