A Geobacter sulfurreducens strain expressing Pseudomonas aeruginosa type IV pili localizes OmcS on pili but is deficient in Fe(III) oxide reduction and current production

Applied and Environmental Microbiology

Volumn 80, Issue 3, 2014, Pages 1219-1224

  Liu, Xing ^a,b   Tremblay, Pier Luc ^a,d   Malvankar, Nikhil S ^a   Nevin, Kelly P ^a   Lovley, Derek R ^a   Vargas, Madeline ^a,c  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b SOUTHEAST UNIVERSITY   (China)

^c Department of Biology   (United States)

^d Chalmers University of Technology   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

C-TYPE CYTOCHROME; CURRENT PRODUCTION; ELECTRON TRANSFER; ELECTRON TRANSPORT; GEOBACTER SULFURREDUCENS; OXIDE REDUCTION; PSEUDOMONAS AERUGINOSA; STRUCTURAL FEATURE;

ELECTRON TRANSITIONS; ELECTRON TRANSPORT PROPERTIES; GENES;

BACTERIA;

BACTERIUM; BIOFILM; CYTOCHROME; ELECTRICAL CONDUCTIVITY; ELECTRON; FUNCTIONAL ROLE; GENE EXPRESSION; IRON OXIDE; PROTEIN; REDUCTION;

CYTOCHROME C; FERRIC ION; FIMBRIA PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ELECTRICITY; FIMBRIA; GENETICS; GEOBACTER; METABOLISM; METHANOSARCINACEAE; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PSEUDOMONAS AERUGINOSA; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; CYTOCHROMES C; ELECTRICITY; FERRIC COMPOUNDS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GEOBACTER; METHANOSARCINACEAE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PSEUDOMONAS AERUGINOSA; SEQUENCE ALIGNMENT;

EID: 84893012980     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02938-13     Document Type: Article

References (32)

1. Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru A-E, Holmes DE, Franks AE, Orellana R, Risso C, Nevin KP. 2011. Geobacter: the microbe electric's physiology, ecology, and practical applications. Adv. Microb. Physiol. 59:1-100. http://dx.doi.org/10.1016/B978-0-12-387661-4.00004-5.
2. Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim BC, Inoue K, Mester T, Covalla SF, Johnson JP, Rotello VM, Tuominen MT, Lovley DR. 2011. Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 6:573-579. http://dx.doi.org/10 .1038/nnano.2011.119.
3. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR. 2005. Extracellular electron transfer via microbial nanowires. Nature 435:1098-1101. http://dx.doi.org/10.1038/nature03661.
4. Lovley DR. 2011. Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energy Environ. Sci. 4:4896-4906. http://dx.doi.org/10.1039/c1ee02229f.
5. Bonanni PS, Massazza D, Busalmen JP. 2013. Stepping stones in the electron transport from cells to electrodes in Geobacter sulfurreducens biofilms. Phys. Chem. Chem. Phys. 15:10300-10306. http://dx.doi.org/10 .1039/c3cp50411e.
6. Malvankar NS, Lovley DR. 2012. Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. ChemSusChem 5:1039-1046. http://dx.doi.org/10.1002/cssc.201100733.
7. Vargas M, Malvankar NS, Tremblay P-L, Leang C, Smith JA, Patel P, Synoeyenbos-West O, Nevin KP, Lovley DR. 2013. Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio 4(2):e00105-13. http://dx.doi .org/10.1128/mBio.00105-13.
8. Feliciano GT, da Silva AJR, Reguera G, Artacho E. 2012. Molecular and electronic structure of the peptide subunit of Geobacter sulfurreducens conductive pili from first principles. J. Phys. Chem. A 116:8023-8030. http://dx.doi.org/10.1021/jp302232p.
9. Leang C, Qian X, Mester T, Lovley DR. 2010. Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl. Environ. Microbiol. 76:4080-4084. http://dx.doi.org/10.1128/AEM.00023-10.
10. Malvankar NS, Tuominen MT, Lovley DR. 2012. Lack of cytochrome involvement in long-range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens. Energy Environ. Sci. 5:8651-8659. http://dx.doi.org/10.1039/c2ee22330a.
11. Pirbadian S, El-Naggar MY. 2012. Multistep hopping and extracellular charge transfer in microbial redox chains. Phys. Chem. Chem. Phys. 14: 13802-13808. http://dx.doi.org/10.1039/c2cp41185g.
12. El-Naggar MY, Wanger G, Leung KM, Yuzvinsky TD, Southam G, Yang J, Lau WM, Nealson KH, Gorby YA. 2010. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc. Natl. Acad. Sci. U. S. A. 107:18127-18131. http://dx.doi.org/10.1073/pnas.1004880107.
13. Reardon PN, Mueller KT. 2013. Structure of the type IVa major pilin from the electrically conductive bacterial nanowires of Geobacter sulfurreducens. J. Biol. Chem. 288:29260-29266. http://dx.doi.org/10.1074/jbc .M113.498527.
14. Craig L, Pique ME, Tainer JA. 2004. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2:363-378. http://dx.doi.org/10.1038 /nrmicro885.
15. Burrows LL. 2012. Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu. Rev. Microbiol. 66:493-520. http://dx.doi.org/10 .1146/annurev-micro-092611-150055.
16. Mattick JS, Bills MM, Anderson BJ, Dalrymple B, Mott MR, Egerton JR. 1987. Morphogenetic expression of Bacteroides nodosus fimbriae in Pseudomonas aeruginosa. J. Bacteriol. 169:33-41.
17. Beard MK, Mattick JS, Moore LJ, Mott MR, Marrs CF, Egerton JR. 1990. Morphogenetic expression of Moraxella bovis fimbriae (pili) in Pseudomonas aeruginosa. J. Bacteriol. 172:2601-2607.
18. Hoyne PA, Haas R, Meyer TF, Davies JK, Elleman TC. 1992. Production of Neisseria gonorrhoeae pili (fimbriae) in Pseudomonas aeruginosa. J. Bacteriol. 174:7321-7327.
19. Coppi MV, Leang C, Sandler SJ, Lovley DR. 2001. Development of a genetic system for Geobacter sulfurreducens. Appl. Environ. Microbiol. 67:3180-3187. http://dx.doi.org/10.1128/AEM.67.7.3180-3187.2001.
20. Lovley DR, Phillips EJP. 1988. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54:1472-1480.
21. Risso C, Methé BA, Elifantz H, Holmes DE, Lovley DR. 2008. Highly conserved genes in Geobacter species with expression patterns indicative of acetate limitation. Microbiology 154:2589-2599. http://dx.doi.org/10 .1099/mic.0.2008/017244-0.
22. Mehta T, Coppi MV, Childers SE, Lovley DR. 2005. Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71:8634-8641. http: //dx.doi.org/10.1128/AEM.71.12.8634-8641.2005.
23. Thomas PE, Ryan D, Levin W. 1976. An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal. Biochem. 75:168-176. http: //dx.doi.org/10.1016/0003-2697(76)90067-1.
24. Giltner CL, Habash M, Burrows LL. 2010. Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J. Mol. Biol. 398:444-461. http://dx.doi.org/10.1016/j.jmb.2010.03.028.
25. Nevin KP, Kim B-C, Glaven RH, Johnson JP, Woodard TL, Methé BA, DiDonato RJ, Jr, Covalla SF, Franks AE, Liu A, Lovley DR. 2009. Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS One 4:e5628. http://dx.doi.org/10.1371/journal.pone.0005628.
26. Franks AE, Nevin KP, Glaven RH, Lovley DR. 2010. Microtoming coupled to microarray analysis to evaluate the spatial metabolic status of Geobacter sulfurreducens biofilms. ISME J. 4:509-519. http://dx.doi.org /10.1038/ismej.2009.137.
27. Nevin KP, Zhang P, Franks AE, Woodard TL, Lovley DR. 2011. Anaerobes unleashed: aerobic fuel cells of Geobacter sulfurreducens. J. Power Sources 196:7514-7518. http://dx.doi.org/10.1016/j.jpowsour.2011.05.021.
28. Craig L, Li J. 2008. Type IV pili: paradoxes in form and function. Curr. Opin. Struct. Biol. 18:267-277. http://dx.doi.org/10.1016/j.sbi.2007.12.009.
29. Inoue K, Leang C, Franks AE, Woodard TL, Nevin KP, Lovley DR. 2011. Specific localization of the c-type cytochrome OmcZ at the anode surface in current-producing biofilms of Geobacter sulfurreducens. Environ. Microbiol. Rep. 3:211-217. http://dx.doi.org/10.1111/j.1758-2229 .2010.00210.x.
30. Qian X, Mester T, Morgado L, Arakawa T, Sharma ML, Inoue K, Joseph C, Salgueiro CA, Maroney MJ, Lovley DR. 2011. Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens. Biochim. Biophys. Acta 1807:404-412. http://dx.doi.org/10.1016/j.bbabio.2011.01.003.
31. Lovley DR. 2012. Long-range electron transport to Fe(III) oxide via pili with metallic-like conductivity. Biochem. Soc. Trans. 40:1186-1190. http: //dx.doi.org/10.1042/BST20120131.
32. Lovley DR. 2012. Electromicrobiology. Annu. Rev. Microbiol. 66:391-409. http://dx.doi.org/10.1146/annurev-micro-092611-150104.