A Proteomic View at the Biochemistry of Syntrophic Butyrate Oxidation in Syntrophomonas wolfei

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Schmidt, Alexander ^a   Müller, Nicolai ^a,b   Schink, Bernhard ^a   Schleheck, David ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRYL COENZYME A DEHYDROGENASE; FLAVOPROTEIN; HYDROGENASE; OXIDOREDUCTASE;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIUM CULTURE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; GENE EXPRESSION; MASS SPECTROMETRY; NONHUMAN; OXIDATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEOMICS; SYNTROPHOMONAS WOLFEI; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ACYL COENZYME A; BACTERIA; BACTERIAL PROTEINS; BUTYRATES; ENZYME ACTIVATION; FORMATE DEHYDROGENASES; MASS SPECTROMETRY; MEMBRANE PROTEINS; METHANOSPIRILLUM; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PROTEIN TRANSPORT; PROTEOME; PROTEOMICS;

EID: 84874499699     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056905     Document Type: Article

References (54)

1. Schink B, (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61: 262-280.
2. Sieber JR, McInerney MJ, Gunsalus RP, (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66: 429-452.
3. Müller N, Worm P, Schink B, Stams AJ, Plugge CM, (2010) Syntrophic butyrate and propionate oxidations processes: from genomes to reaction mechanisms. Environ Microbiol Rep 2: 489-499.
4. McInerney MJ (1986) Transient and persistent associations among prokaryotes. In: Pointdexter JS, Leadbetter ER, editors. Bacteria in nature. New York: Plenum Press. pp. 293-338.
5. McInerney MJ (1988) Anaerobic degradation of proteins and lipids. In: Zehnder AJB, editor. Biology of anaerobic microorganisms. New York: John Wiley & Sons. pp. 374-415.
6. Thauer RK, Jungermann K, Decker K, (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41: 100-180.
7. Gustafson WG, Feinberg BA, McFarland JT, (1986) Energetics of beta-oxidation. Reduction potentials of general fatty acyl-CoA dehydrogenase, electron transfer flavoprotein, and fatty acyl-CoA substrates. J Biol Chem 261: 7733-7741.
8. Wofford NQ, Beaty PS, McInerney MJ, (1986) Preparation of cell-free extracts and the enzymes involved in fatty acid metabolism in Syntrophomonas wolfei. J Bacteriol 167: 179-185.
9. McInerney MJ, Wofford NQ, (1992) Enzymes involved in crotonate metabolism in Syntrophomonas wolfei. Arch Microbiol 158: 344-349.
10. Sato K, Nishina Y, Setoyama C, Miura R, Shiga K, (1999) Unusually high standard redox potential of acrylyl-CoA/propionyl-CoA couple among enoyl-CoA/acyl-CoA couples: a reason for the distinct metabolic pathway of propionyl-CoA from longer acyl-CoAs. J Biochem 126: 668-675.
11. Wallrabenstein C, Schink B, (1994) Evidence of reversed electron transport in syntrophic butyrate or benzoate oxidation by Syntrophomonas wolfei and Syntrophus buswellii. Arch Microbiol 162: 136-142.
12. Sieber JR, Sims DR, Han C, Kim E, Lykidis A, et al. (2010) The genome of Syntrophomonas wolfei: new insights into syntrophic metabolism and biohydrogen production. Environ Microbiol 12: 2289-2301.
13. Schut GJ, Adams MW, (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191: 4451-4457.
14. Müller N, Schleheck D, Schink B, (2009) Involvement of NADH:acceptor oxidoreductase and butyryl coenzyme A dehydrogenase in reversed electron transport during syntrophic butyrate oxidation by Syntrophomonas wolfei. J Bacteriol 191: 6167-6177.
15. Schäffer C, Messner P, (2004) Surface-layer glycoproteins: an example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology. Glycobiology 14: 31-42.
16. Jones RW, Gray TA, Garland PB, (1976) A study of the permeability of the cytoplasmic membrane of Escherichia coli to reduced and oxidized benzyl viologen and methyl viologen cations: complications in the use of viologens as redox mediators for membrane-bound enzymes. Biochem Soc Trans 4: 671-673.
17. McInerney MJ, Bryant MP, Pfennig N, (1979) Anaerobic bacterium that degrades fatty acids in syntrophic association with methanogens. Arch Microbiol 122: 129-135.
18. Sato K, Nishina Y, Shiga K, (2003) Purification of electron-transferring flavoprotein from Megasphaera elsdenii and binding of additional FAD with an unusual absorption spectrum. J Biochem 134: 719-729.
19. Falke D, Schulz K, Doberenz C, Beyer L, Lilie H, et al. (2010) Unexpected oligomeric structure of the FocA formate channel of Escherichia coli: a paradigm for the formate-nitrite transporter family of integral membrane proteins. FEMS Microbiol Lett 303: 69-75.
20. Worm P, Stams AJM, Cheng X, Plugge CM, (2011) Growth- and substrate-dependent transcription of formate dehydrogenase and hydrogenase coding genes in Syntrophobacter fumaroxidans and Methanospirillum hungatei. Microbiology 157: 280-289.
21. Rahlfs S, Müller V, (1997) Sequence of subunit c of the Na+-translocating F1F0 ATPase of Acetobacterium woodii: proposal for determinants of Na+ specificity as revealed by sequence comparisons. FEBS Letters 404: 269-271.
22. Dzioba J, Häse CC, Gosink K, Galperin MY, Dibrov P, (2003) Experimental verification of a sequence-based prediction: F1F0-type ATPase of Vibrio cholerae transports protons, not Na+ ions. J Bacteriol 185: 674-678.
23. Biel S, Simon J, Gross R, Ruiz T, Ruitenberg M, et al. (2002) Reconstitution of coupled fumarate respiration in liposomes by incorporating the electron transport enzymes isolated from Wolinella succinogenes. Eur J Biochem 269: 1974-1983.
24. Kröger A, Biel S, Simon J, Gross R, Unden G, et al. (2002) Fumarate respiration of Wolinella succinogenes: enzymology, energetics and coupling mechanism. Biochim Biophys Acta 1553: 23-38.
25. Beveridge TJ, Pouwels PH, Sára M, Kotiranta A, Lounatmaa K, et al. (1997) V. Functions of S-layers. FEMS Microbiol Rev 20: 99-149.
26. Sleytr UB, Beveridge TJ, (1999) Bacterial S-layers. Trends Microbiol 7: 253-260.
27. Engelhardt H, (2007) Are S-layers exoskeletons? The basic function of protein surface layers revisited. J Struct Biol 160: 115-124.
28. Zhao HX, Yang DC, Woese CR, Bryant MP, (1990) Assignment of Clostridium bryantii to Syntrophospora bryantii gen. nov., comb. nov. on the basis of a 16S rRNA sequence analysis of its crotonate-grown pure culture. Int J Syst Bacteriol 40: 40-44.
29. McInerney MJ, Bryant MP, Hespell RB, Costerton JW, (1981) Syntrophomonas wolfei gen. nov. sp. nov., an anaerobic, syntrophic, fatty acid-oxidizing bacterium. Appl Environ Microbiol 41: 1029-1039.
30. Calamita HG, Ehringer WD, Koch AL, Doyle RJ, (2001) Evidence that the cell wall of Bacillus subtilis is protonated during respiration. Proc Natl Acad Sci U S A 98: 15260-15263.
31. Calamita HG, Doyle RJ, (2002) Regulation of autolysins in teichuronic acid-containing Bacillus subtilis cells. Mol Microbiol 44: 601-606.
32. Biswas R, Martinez RE, Göhring N, Schlag M, Josten M, et al. (2012) Proton-binding capacity of Staphylococcus aureus wall teichoic acid and its role in controlling autolysin activity. PLoS ONE 7: e41415.
33. Sára M, Sleytr UB, (2000) S-Layer proteins. J Bacteriol 182: 859-868.
34. Lee JW, (2012) Proton-electrostatics hypothesis for localized proton coupling bioenergetics. Bioenergetics 1: e104.
35. Beaty PS, McInerney MJ, (1989) Effects of organic acid anions on the growth and metabolism of Syntrophomonas wolfei in pure culture and in defined consortia. Appl Environ Microbiol 55: 977-983.
36. McInerney MJ, Mackie RI, Bryant MP, (1981) Syntrophic association of a butyrate-degrading bacterium and methanosarcina enriched from bovine rumen fluid. Appl Environ Microbiol 41: 826-828.
37. Widdel F, Bak F (1992) Gram-negative mesophilic sulfate-reducing bacteria. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH, editors. The prokaryotes. Berlin: Springer Verlag. pp. 3352-3378.
38. Widdel F, Kohring GW, Mayer F, (1983) Studies on dissimilatrory sulfate-reducing bacteria that decompose fatty acids. III. Characterization of filamentous gliding Desulfonema limicola gen. nov. sp. nov, and Desulfonema magnum sp. nov. Arch Microbiol 134: 286-294.
39. Müller N, Griffin BM, Stingl U, Schink B, (2008) Dominant sugar utilizers in sediment of Lake Constance depend on syntrophic cooperation with methanogenic partner organisms. Environ Microbiol 10: 1501-1511.
40. Beaty PS, McInerney MJ, (1990) Nutritional features of Syntrophomonas wolfei. Appl Environ Microbiol 56: 3223-3224.
41. Beaty PS, Wofford NQ, McInerney MJ, (1987) Separation of Syntrophomonas wolfei from Methanospirillum hungatii in syntrophic cocultures by using percoll gradients. Appl Environ Microbiol 53: 1183-1185.
42. McKellar RC, Sprott GD, (1979) Solubilization and properties of a paniculate hydrogenase from Methanobacterium strain G2R. J Bacteriol pp. 231-238.
43. Bergmeyer HU, (1975) New values for the molar extinction coefficients of NADH and NADPH for the use in routine laboratories. Z Klin Chem Klin Biochem 13: 507-508.
44. Diekert GB, Thauer RK, (1978) Carbon monoxide oxidation by Clostridium thermoaceticum and Clostridium formicoaceticum. J Bacteriol 136: 597-606.
45. Bradford M, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
46. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature Methods 227: 680-685.
47. Neuhoff V, Arold N, Taube D, Ehrhardt W, (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255-262.
48. Wittig I, Braun HP, Schagger H, (2006) Blue native PAGE. Nature Protocols 1: 418-428.
49. Perkins DN, Pappin DJC, Creasy DM, Cottrell JS, (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
50. Marchler-Bauer A, Bryant SH, (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: 327-331.
51. Geer LY, Domrachev M, Lipman DJ, Bryant SH, (2002) CDART: protein homology by domain architecture. Genome Res 12: 1619-1623.
52. Petersen TN, Brunak S, von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8: 785-786.
53. Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S, (2005) Prediction of twin-arginine signal peptides. BMC bioinformatics 6: 167.
54. Bagos PG, Nikolaou EP, Liakopoulos TD, Tsirigos KD, (2010) Combined prediction of Tat and Sec signal peptides with Hidden Markov Models. Bioinformatics 26: 2811-2817.