The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism

Environmental Microbiology

Volumn 16, Issue 1, 2014, Pages 177-188

  Sieber, Jessica R ^a   Le, Huynh M ^a   Mcinerney, Michael J ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHANOSPIRILLUM HUNGATEI; SYNTROPHOMONAS WOLFEI; SYNTROPHUS ACIDITROPHICUS;

BACTERIAL PROTEIN; BENZOIC ACID DERIVATIVE; BUTYRIC ACID DERIVATIVE; FORMATE DEHYDROGENASE; FORMIC ACID; FORMIC ACID DERIVATIVE; HYDROGEN; HYDROGENASE; METHANE;

ARTICLE; BACTERIUM; DELTAPROTEOBACTERIA; ELECTRON TRANSPORT; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATION REDUCTION REACTION;

BACTERIA; BACTERIAL PROTEINS; BENZOATES; BUTYRATES; DELTAPROTEOBACTERIA; ELECTRON TRANSPORT; FORMATE DEHYDROGENASES; FORMATES; HYDROGEN; HYDROGENASE; METHANE; OXIDATION-REDUCTION;

EID: 84891624031     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12269     Document Type: Article

References (68)

1. Anderson, S., Lyle, I., and Paterson, R. (1976) Electron transfer across membranes using vitamin K1 and coenzyme Q10 as carrier molecules. Nature 259: 147-148.
2. Balch, W., and Wolfe, R. (1976) New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl Environ Microbiol 32: 781-791.
3. Beaty, P.S., and McInerney, M.J. (1987) Growth of Syntrophomonas wolfei in pure culture on crotonate. Arch Microbiol 147: 389-393.
4. Beaty, P.S., Wofford, N.Q., and McInerney, M.J. (1987) Separation of Syntrophomonas wolfei from Methanospirillum hungatei in syntrophic cocultures by using percoll gradients. Appl Environ Microbiol 53: 1183-1185.
5. Boetius, A., Ravenschlag, K., Schubert, C.J., Rickert, D., Widdel, F., Gieseke, A., etal. (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407: 623-626.
6. de Bok, F.A., Roze, E.H., and Stams, A.J. (2002a) Hydrogenases and formate dehydrogenases of Syntrophobacter fumaroxidans. Antonie van Leeuwenhoek 81: 283-291.
7. de Bok, F.A., Luijten, M.L., and Stams, A.J. (2002b) Biochemical evidence for formate transfer in syntrophic propionate-oxidizing cocultures of Syntrophobacter fumaroxidans and Methanospirillum hungatei. Appl Environ Microbiol 68: 4247-4252.
8. 2-reductases) involved in syntrophic propionate oxidation by Syntrophobacter fumaroxidans. Eur J Biochem 270: 2476-2485.
9. Bradford, M.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.
10. Clemente, J.S., and Fedorak, P.M. (2005) A review of the occurrence, analyses, toxicity, and biodegradation of naphthenic acids. Chemosphere 60: 585-600.
11. Conrad, R., Phelps, T., and Zeikus, J. (1985) Gas metabolism evidence in support of the juxtaposition of hydrogen-producing and methanogenic bacteria in sewage sludge and lake sediments. Appl Environ Microbiol 50: 595-601.
12. Cozzarelli, I.M., Eganhouse, R.P., and Baedecker, M.J. (1990) Transformation of monoaromatic hydrocarbons to organic acids in anoxic groundwater environment. Environ Geol 16: 135-141.
13. 2 and formate formation during syntrophic butyrate and propionate degradation. Anaerobe 1: 35-39.
14. Elshahed, M.S., and McInerney, M.J. (2001) Benzoate fermentation by the anaerobic bacterium Syntrophus aciditrophicus in the absence of hydrogen-using microorganisms. Appl Environ Microbiol 67: 5520-5525.
15. Farkas, L., and Fischer, E. (1947) On the activation of molecular hydrogen by Proteus vulgaris. J Biol Chem 167: 787-805.
16. Gage, J. (1968) The action of paraquat and diquat on the respiration of liver cell fractions. Biochem J 109: 757-761.
17. Gorby, Y.A., Yanina, S., McLean, J.S., Rosso, K.M., Moyles, D., and Dohnalkova, A. (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci USA 103: 11358-11363.
18. Hatamoto, M., Imachi, H., Ohashi, A., and Harada, H. (2007a) Identification and cultivation of anaerobic, syntrophic long-chain fatty acid-degrading microbes from mesophilic and thermophilic methanogenic sludges. Appl Environ Microbiol 73: 1332-1340.
19. Hatamoto, M., Imachi, H., Yashiro, Y., Ohashi, A., and Harada, H. (2007b) Diversity of anaerobic microorganisms involved in long-chain fatty acid degradation in methanogenic sludges as revealed by RNA-based stable isotope probing. Appl Environ Microbiol 73: 4119-4127.
20. Hauska, G., Reimer, S., and Trebst, A. (1974) Native and artificial energy-conserving sites in cyclic photophosphorylation systems. BBA-Bioenergetics 357: 1-13.
21. Heider, J., and Fuchs, G. (1997) Microbial anaerobic aromatic metabolism. Anaerobe 3: 1-22.
22. Hoberman, H.D., and Rittenberg, D. (1943) Biological catalysis of the exchange reaction between water and hydrogen. J Biol Chem 147: 211-227.
23. Ishii, S., Kosaka, T., Hori, K., Hotta, Y., and Watanabe, K. (2005) Coaggregation facilitates interspecies hydrogen transfer between Pelotomaculum thermopropionicum and Methanothermobacter thermautotrophicus. Appl Environ Microbiol 71: 7838-7845.
24. Jackson, B.E., and McInerney, M.J. (2002) Anaerobic microbial metabolism can proceed close to thermodynamic limits. Nature 415: 454-456.
25. Jackson, B.E., Bhupathiraju, V.K., Tanner, R.S., Woese, C.R., and McInerney, M.J. (1999) Syntrophus aciditrophicus sp. nov., a new anaerobic bacterium that degrades fatty acids and benzoate in syntrophic association with hydrogen-using microorganisms. Arch Microbiol 171: 107-114.
26. Jones, D.M., Head, I.M., Gray, N.D., Adams, J.J., Rowan, A.K., Aitken, C.M., etal. (2008) Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451: 176-180.
27. Jones, R.W., and Garland, P.B. (1977) Sites and specificity of the reaction of bipyridylium compounds with anaerobic respiratory enzymes of Escherichia coli. Effects of permeability barriers imposed by the cytoplasmic membrane. Biochem J 164: 199-211.
28. 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.
29. Leang, C., Qian, X., Mester, T., and Lovley, D.R. (2010) Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl Environ Microbiol 76: 4080-4084.
30. Liu, G., Zhang, R., El-Mashad, H.M., Dong, R., and Liu, X. (2011) Biogasification of green and food wastes using anaerobic-phased solids digester system. Appl Biochem Biotechnol 168: 78-90.
31. McInerney, M.J., Bryant, M.P., and Pfennig, N. (1979) Anaerobic bacterium that degrades fatty acids in syntrophic association with methanogens. Arch Microbiol 122: 129-135.
32. McInerney, M.J., Bryant, M.P., Hespell, R.B., and Costerton, J.W. (1981) Syntrophomonas wolfei gen. nov. sp. nov., an anaerobic, syntrophic, fatty acid-oxidizing bacterium. Appl Environ Microbiol 41: 1029-1039.
33. McInerney, M.J., Rohlin, L., Mouttaki, H., Kim, U., Krupp, R.S., Rios-Hernandez, L., etal. (2007) The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth. Proc Natl Acad Sci USA 104: 7600-7605.
34. McInerney, M.J., Struchtemeyer, C.G., Sieber, J., Mouttaki, H., Stams, A.J.M., Schink, B., etal. (2008) Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. In Incredible Anaerobes From Physiology to Genomics to Fuels. Wiegel, J., Maier, R.J., and Adams, M.W. (eds). Ann N Y Acad Sci, Boston, MA, USA: Blackwell Publishing, pp. 58-72.
35. McInerney, M.J., Sieber, J.R., and Gunsalus, R.P. (2009) Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20: 623-632.
36. 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.
37. Meyer, B., Kuehl, J., Deutschbauer, A.M., Price, M.N., Arkin, A.P., and Stahl, D.A. (2013) Variation among Desulfovibrio species in electron transfer systems used for syntrophic growth. J Bacteriol 195: 990-1004.
38. Morita, M., Malvankar, N.S., Franks, A.E., Summers, Z.M., Giloteaux, L., Rotaru, A.E., etal. (2011) Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. mBio 2: doi: 10.1128/mBio.00159-11.
39. Mouttaki, H., Nanny, M.A., and McInerney, M.J. (2007) Cyclohexane carboxylate and benzoate formation from crotonate in Syntrophus aciditrophicus. Appl Environ Microbiol 73: 930-938.
40. Mouttaki, H., Nanny, M.A., and McInerney, M.J. (2008) Use of benzoate as an electron acceptor by Syntrophus aciditrophicus grown in pure culture with crotonate. Environ Microbiol 10: 3265-3274.
41. Müller, N., Schleheck, D., and 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.
42. Müller, N., Worm, P., Schink, B., Stams, A.J., and Plugge, C.M. (2010) Syntrophic butyrate and propionate oxidation processes: from genomes to reaction mechanisms. Environ Microbiol Rep 2: 489-499.
43. Nielsen, L.P., Risgaard-Petersen, N., Fossing, H., Christensen, P.B., and Sayama, M. (2010) Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463: 1071-1074.
44. Odom, J.M., and Peck, H.D., Jr (1981) Localization of dehydrogenases, reductases, and electron transfer components in the sulfate-reducing bacterium Desulfovibrio gigas. J Bacteriol 147: 161-169.
45. Pavlostathis, S.G., and Giraldo-Gomez, E. (1991) Kinetics of anaerobic treatment: a critical review. Crit Rev Environ Control 21: 411-490.
46. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
47. Pfeffer, C., Larsen, S., Song, J., Dong, M., Besenbacher, F., Meyer, R.L., etal. (2012) Filamentous bacteria transport electrons over centimetre distances. Nature 491: 218-221.
48. Reguera, G., McCarthy, K.D., Mehta, T., Nicoll, J.S., Tuominen, M.T., and Lovley, D.R. (2005) Extracellular electron transfer via microbial nanowires. Nature 435: 1098-1101.
49. Rotaru, A.-E., Shrestha, P.M., Liu, F., Ueki, T., Nevin, K., Summers, Z.M., and Lovley, D.R. (2012) Interspecies electron transfer via hydrogen and formate rather than direct electrical connections in cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens. Appl Environ Microbiol 78: 7645-7651.
50. Saha, S., Ouitrakul, R., Izawa, S., and Good, N. (1971) Electron transport and photophosphorylation in chloroplasts as a function of the electron acceptor. J Biol Chem 246: 3204-3209.
51. Schink, B. (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61: 262-280.
52. Schink, B. (2006) Syntrophic associations in methanogenic degradation. Prog Mol Subcell Biol 41: 1-19.
53. Schmidt, A., Müller, N., Schink, B., and Schleheck, D. (2013) A proteomic view at the biochemistry of syntrophic butyrate oxidation in Syntrophomonas wolfei. PLoS ONE 8: e56905.
54. Schut, G., and Adams, M. (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191: 4451-4457.
55. Shimoyama, T., Kato, S., Ishii, S., and Watanabe, K. (2009) Flagellum mediates symbiosis. Science 323: 1574.
56. Shrestha, P.M., Rotaru, A.-E., Summers, Z.M., Shrestha, M., Liu, F., and Lovley, D.R. (2013) Transcriptomic and genetic analysis of direct interspecies electron transfer. Appl Environ Microbiol 79: 2397-2404.
57. Sieber, J.R., Sims, D.R., Han, C., Kim, E., Lykidis, A., Lapidus, A.L., etal. (2010) The genome of Syntrophomonas wolfei: new insights into syntrophic metabolism and biohydrogen production. Environ Microbiol 12: 2289-2301.
58. Sieber, J.R., McInerney, M.J., and Gunsalus, R.P. (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Ann Rev Microbiol 66: 429-452.
59. Sousa, D.Z., Smidt, H., Alves, M.M., and Stams, A.J. (2007) Syntrophomonas zehnderi sp. nov., an anaerobe that degrades long-chain fatty acids in co-culture with Methanobacterium formicicum. Int J Syst Evol Microbiol 57: 609-615.
60. Stams, A.J., and Dong, X. (1995) Role of formate and hydrogen in the degradation of propionate and butyrate by defined suspended cocultures of acetogenic and methanogenic bacteria. Antonie van Leeuwenhoek 68: 281-284.
61. Struchtemeyer, C.G., Elshahed, M.S., Duncan, K.E., and McInerney, M.J. (2005) Evidence for aceticlastic methanogenesis in the presence of sulfate in a gas condensate-contaminated aquifer. Appl Environ Microbiol 71: 5348-5353.
62. Struchtemeyer, C.G., Duncan, K.E., and McInerney, M.J. (2011) Evidence for syntrophic butyrate metabolism under sulfate-reducing conditions in a hydrocarbon-contaminated aquifer. FEMS Microbiol Ecol 76: 289-300.
63. 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.
64. Takamiya, A. (1953) Studies on the formic dehydrogenase of Escherichia coli III. Determination of the quantity of the enzyme within the cell by using hypophosphite as a specific inhibitor. J Biochem 40: 407-414.
65. Walker, C.B., He, Z., Yang, Z.K., Ringbauer, J.A., Jr, He, Q., Zhou, J., etal. (2009) The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J Bacteriol 191: 5793-5801.
66. Wofford, N.Q., Beaty, P.S., and McInerney, M.J. (1986) Preparation of cell-free extracts and the enzymes involved in fatty acid metabolism in Syntrophomonas wolfei. J Bacteriol 167: 179-185.
67. Worm, P., Stams, A.J.M., Cheng, X., and Plugge, C.M. (2011) Growth- and substrate-dependent transcription of formate dehydrogenase and hydrogenase coding genes in Syntrophobacter fumaroxidans and Methanospirillum hungatei. Microbiology 157: 280-289.
68. Zengler, K., Richnow, H., Rosselló-Mora, R., Michaelis, W., and Widdel, F. (1999) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401: 266-269.