Changes in phosphorylation of adenosine phosphate and redox state of nicotinamide-adenine dinucleotide (phosphate) in Geobacter sulfurreducens in response to electron acceptor and anode potential variation

Bioelectrochemistry

Volumn 106, Issue , 2015, Pages 213-220

  Rose, Nicholas D ^a   Regan, John M ^a,b  

^a The Pennsylvania State University   (United States)

^b First Environment Inc ^*  (United States)

Author keywords

Adenosine phosphate; Geobacter sulfurreducens; Nicotinamide adenine dinucleotide; Redox potential

Indexed keywords

ADENOSINETRIPHOSPHATE; AMIDES; ANODES; BIOFILMS; ELECTRONS; MOBILE SECURITY; NUCLEOTIDES; PHOSPHATES; PHOSPHORYLATION; REDOX REACTIONS;

ADENOSINE MONOPHOSPHATE; ADENYLATE ENERGY CHARGES; BIO-ELECTROCHEMICAL SYSTEMS; GEOBACTER SULFURREDUCENS; INTRACELLULAR CONCENTRATION; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATES; NICOTINAMIDE ADENINE DINUCLEOTIDES; REDOX POTENTIALS;

ELECTRODES;

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; FERRIC CITRATE; FERRIC ION; FUMARIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; ADENINE NUCLEOTIDE; FUMARIC ACID DERIVATIVE;

ARTICLE; BACTERIAL GROWTH; ELECTRON; GEOBACTER SULFURREDUCENS; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION STATE; PHOSPHORYLATION; BIOFILM; ELECTRODE; ELECTRON TRANSPORT; GEOBACTER; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

ADENINE NUCLEOTIDES; ADENOSINE MONOPHOSPHATE; BIOFILMS; ELECTRODES; ELECTRON TRANSPORT; FERRIC COMPOUNDS; FUMARATES; GEOBACTER; NADP; PHOSPHORYLATION;

EID: 84940789851     PISSN: 15675394     EISSN: 1878562X     Source Type: Journal    
DOI: 10.1016/j.bioelechem.2015.03.003     Document Type: Article

References (51)

1. Ying W. NAD+ and NADH in cellular functions and cell death. Front. Biosci. 2006, 11:3129-3148.
2. Ying W. NAD+ and NADH in brain functions, brain diseases and brain aging. Front. Biosci. 2007, 12:1863-1888.
3. Pradet A., Raymond P. Adenine-nucleotide ratios and adenylate energy-charge in energy-metabolism. Annu. Rev. Plant Physiol. 1983, 34:199-224.
4. Atkinson D.E. The energy charge of the adenylate pool as a regulatory parameter, interaction with feedback modifiers. Biochemistry 1968, 7:4030-4034.
5. de Graef M.R., Alexeeva S., Snoep J.L., Teixeira de Mattos M.J. The steady-state internal redox state (NADH/NAD) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli. J. Bacteriol. 1999, 181:2351-2357.
6. Leonardo M.R., Cunningham P.R., Clark D.P. Anaerobic regulation of the adhE gene, encoding the fermentative alcohol dehydrogenase of Escherichia coli. J. Bacteriol. 1993, 175:870-878.
7. Leonardo M.R., Dailly Y., Clark D.P. Role of NAD in regulating the adhE gene of Escherichia coli. J. Bacteriol. 1996, 178:6013-6018.
8. Levanon S.S., San K.Y., Bennett G.N. Effect of oxygen on the Escherichia coli ArcA and FNR regulation systems and metabolic responses. Biotechnol. Bioeng. 2005, 89:556-564.
9. Snoep J.L., Teixeira de Mattos M.J., Postma P.W., Neijssel O.M. Involvement of pyruvate dehydrogenase in product formation in pyruvate-limited anaerobic chemostat cultures of Enterococcus faecalis NCTC 775. Arch. Microbiol. 1990, 154:50-55.
10. Snoep J.L., Joost M., de Mattos T., Neijssel O.M. Effect of the energy source on the NADH/NAD ratio and on pyruvate catabolism in anaerobic chemostat cultures of Enterococcus faecalis NCTC 775. FEMS Microbiol. Lett. 1991, 81:63-66.
11. Girbal L., Soucaille P. Regulation of Clostridium acetobutylicum metabolism as revealed by mixed-substrate steady-state continuous cultures: role of NADH/NAD ratio and ATP pool. J. Bacteriol. 1994, 176:6433-6438.
12. Girbal L., Vasconcelos I., Soucaille P. Transmembrane pH of Clostridium acetobutylicum is inverted (more acidic inside) when the in vivo activity of hydrogenase is decreased. J. Bacteriol. 1994, 176:6146-6147.
13. Meyer C.L., Papoutsakis E.T. Increased levels of ATP and NADH are associated with increased solvent production in continuous cultures of Clostridium acetobutylicum. Appl. Microbiol. Biotechnol. 1989, 30:450-459.
14. Yong Y.-C., Yu Y.-Y., Yang Y., Li C.M., Jiang R., Wang X., Wang J.-Y., Song H. Increasing intracellular releasable electrons dramatically enhances bioelectricity output in microbial fuel cells. Electrochem. Commun. 2012, 19:13-16.
15. Chapman A.G., Fall L., Atkinson D.E. Adenylate energy charge in Escherichia coli during growth and starvation. J. Bacteriol. 1971, 108:1072-1086.
16. Ball W.J., Atkinson D.E. Adenylate energy charge in Saccharomyces cerevisiae during starvation. J. Bacteriol. 1975, 121:975-982.
17. Kiely P.D., Rader G., Regan J.M., Logan B.E. Long-term cathode performance and the microbial communities that develop in microbial fuel cells fed different fermentation endproducts. Bioresour. Technol. 2011, 102:361-366.
18. Jung S., Regan J.M. Comparison of anode bacterial communities and performance in microbial fuel cells with different electron donors. Appl. Microbiol. Biotechnol. 2007, 77:393-402.
19. Call D.F., Wagner R.C., Logan B.E. Hydrogen production by geobacter species and a mixed consortium in a microbial electrolysis cell. Appl. Environ. Microbiol. 2009, 75:7579-7587.
20. Nevin K.P., Richter H., Covalla S.F., Johnson J.P., Woodard T.L., Orloff A.L., Jia H., Zhang M., Lovley D.R. Power output and columbic efficiencies from biofilms of Geobacter sulfurreducens comparable to mixed community microbial fuel cells. Environ. Microbiol. 2008, 10:2505-2514.
21. Caccavo F., Lonergan D.J., Lovley D.R., Davis M., Stolz J.F., McInerney M.J. Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl. Environ. Microbiol. 1994, 60:3752-3759.
22. Hu H., Fan Y., Liu H. Hydrogen production using single-chamber membrane-free microbial electrolysis cells. Water Res. 2008, 42:4172-4178.
23. Marsili E., Rollefson J.B., Baron D.B., Hozalski R.M., Bond D.R. Microbial biofilm voltammetry: direct electrochemical characterization of catalytic electrode-attached biofilms. Appl. Environ. Microbiol. 2008, 74:7329-7337.
24. Inoue K., Qian X., Morgado L., Kim B.C., Mester T., Izallalen M., Salgueiro C.A., Lovley D.R. Purification and characterization of OmcZ, an outer-surface, octaheme c-type cytochrome essential for optimal current production by Geobacter sulfurreducens. Appl. Environ. Microbiol. 2010, 76:3999-4007.
25. Qian X., Mester T., Morgado L., Arakawa T., Sharma M.L., Inoue K., Joseph C., Salgueiro C.A., Maroney M.J., Lovley D.R. Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens. Biochim. Biophys. Acta 2011, 1807:404-412.
26. Marsili E., Sun J., Bond D.R. Voltammetry and growth physiology of Geobacter sulfurreducens biofilms as a function of growth stage and imposed electrode potential. Electroanalysis 2010, 22:865-874.
27. Margarida Martins A., Sha W., Evans C., Martino-Catt S., Mendes P., Shulaev V. Comparison of sampling techniques for parallel analysis of transcript and metabolite levels in Saccharomyces cerevisiae. Yeast 2007, 24:181-188.
28. Lilius E.M., Multanen V.M., Toivonen V. Quantitative extraction and estimation of intracellular nicotinamide nucleotides of Escherichia coli. Anal. Biochem. 1979, 99:22-27.
29. Lundin A., Thore A. Comparison of methods for extraction of bacterial adenine nucleotides determined by firefly assay. Appl. Microbiol. 1975, 30:713-721.
30. Gibon Y., Larher F. Cycling assay for nicotinamide adenine dinucleotides: NaCl precipitation and ethanol solubilization of the reduced tetrazolium. Anal. Biochem. 1997, 251:153-157.
31. Khankal R., Chin J.W., Ghosh D., Cirino P.C. Transcriptional effects of CRP* expression in Escherichia coli. J. Biol. Eng. 2009, 3:13.
32. Ren Z., Ward T.E., Logan B.E., Regan J.M. Characterization of the cellulolytic and hydrogen-producing activities of six mesophilic Clostridium species. J. Appl. Microbiol. 2007, 103:2258-2266.
33. Stookey L.L. Ferrozine-a new spectrophotometric reagent for iron. Anal. Chem. 1970, 42:779-781.
34. Holmes D.E., Chaudhuri S.K., Nevin K.P., Mehta T., Methe B.A., Liu A., Ward J.E., Woodard T.L., Webster J., Lovley D.R. Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ. Microbiol. 2006, 8:1805-1815.
35. Holmes D.E., Nevin K.P., O'Neil R.A., Ward J.E., Adams L.A., Woodard T.L., Vrionis H.A., Lovley D.R. Potential for quantifying expression of the Geobacteraceae citrate synthase gene to assess the activity of Geobacteraceae in the subsurface and on current-harvesting electrodes. Appl. Environ. Microbiol. 2005, 71:6870-6877.
36. Wei J., Liang P., Cao X., Huang X. A new insight into potential regulation on growth and power generation of Geobacter sulfurreducens in microbial fuel cells based on energy viewpoint. Environ. Sci. Technol. 2010, 44:3187-3191.
37. Renslow R.S., Babauta J.T., Dohnalkova A.C., Boyanov M.I., Kemner K.M., Majors P.D., Fredrickson J.K., Beyenal H. Metabolic spatial variability in electrode-respiring Geobacter sulfurreducens biofilms. Energy Environ. Sci. 2013, 6:1827-1836.
38. Lovley D.R., Giovannoni S.J., White D.C., Champine J.E., Phillips E.J., Gorby Y.A., Goodwin S. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch. Microbiol. 1993, 159:336-344.
39. London J., Knight M. Concentrations of nicotinamide nucleotide coenzymes in micro-organisms. J. Gen. Microbiol. 1966, 44:241-254.
40. Leang C., Coppi M.V., Lovley D.R. OmcB, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 2003, 185:2096-2103.
41. Wimpenny J.W., Firth A. Levels of nicotinamide adenine dinucleotide and reduced nicotinamide adenine dinucleotide in facultative bacteria and the effect of oxygen. J. Bacteriol. 1972, 111:24-32.
42. Magnuson T.S., Isoyama N., Hodges-Myerson A.L., Davidson G., Maroney M.J., Geesey G.G., Lovley D.R. Isolation, characterization and gene sequence analysis of a membrane-associated 89kDa Fe(III) reducing cytochrome c from Geobacter sulfurreducens. Biochem. J. 2001, 359:147-152.
43. Galushko A.S., Schink B. Oxidation of acetate through reactions of the citric acid cycle by Geobacter sulfurreducens in pure culture and in syntrophic coculture. Arch. Microbiol. 2000, 174:314-321.
44. Butler J.E., Glaven R.H., Esteve-Nunez A., Nunez C., Shelobolina E.S., Bond D.R., Lovley D.R. Genetic characterization of a single bifunctional enzyme for fumarate reduction and succinate oxidation in Geobacter sulfurreducens and engineering of fumarate reduction in Geobacter metallireducens. J. Bacteriol. 2006, 188:450-455.
45. Esteve-Nunez A., Rothermich M., Sharma M., Lovley D. Growth of Geobacter sulfurreducens under nutrient-limiting conditions in continuous culture. Environ. Microbiol. 2005, 7:641-648.
46. Mahadevan R., Bond D.R., Butler J.E., Esteve-Nunez A., Coppi M.V., Palsson B.O., Schilling C.H., Lovley D.R. Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. Appl. Environ. Microbiol. 2006, 72:1558-1568.
47. Mahadevan R., Yan B., Postier B., Nevin K.P., Woodard T.L., O'Neil R., Coppi M.V., Methe B.A., Krushkal J. Characterizing regulation of metabolism in Geobacter sulfurreducens through genome-wide expression data and sequence analysis. OMICS 2008, 12:33-59.
48. Bagnara A.S., Finch L.R. Quantitative extraction and estimation of intracellular nucleoside triphosphates of Escherichia coli. Anal. Biochem. 1972, 45:24-34.
49. Wiebe W.J., Bancroft K. Use of adenylate energy charge ratio to measure growth state of natural microbial communities. Proc. Natl. Acad. Sci. U. S. A. 1975, 72:2112-2115.
50. Cole H.A., Wimpenny J.W., Hughes D.E. The ATP pool in Escherichia coli. I. Measurement of the pool using modified luciferase assay. Biochim. Biophys. Acta 1967, 143:445-453.
51. Saville R.M., Rakshe S., Haagensen J.A., Shukla S., Spormann A.M. Energy-dependent stability of Shewanella oneidensis MR-1 biofilms. J. Bacteriol. 2011, 193:3257-3264.