Autotrophy at the thermodynamic limit of life: A model for energy conservation in acetogenic bacteria

Nature Reviews Microbiology

Volumn 12, Issue 12, 2014, Pages 809-821

  Schuchmann, Kai ^a   Müller, Volker ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ACETYL COENZYME A; CARBON DIOXIDE; CARBON MONOXIDE; FERREDOXIN; GLUCOSE; METHYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXIDOREDUCTASE; OXYGEN; PHOSPHATE ACETYLTRANSFERASE; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TETRAHYDROFOLIC ACID; ACETIC ACID DERIVATIVE;

ACETOGENIC BACTERIA; AUTOTROPHY; BACTERIUM; BIOCHEMISTRY; CELL MEMBRANE; CHEMICAL REACTION; ELECTRON TRANSPORT; ENERGY CONSERVATION; ENERGY METABOLISM; MOLECULAR WEIGHT; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; REVIEW; STOICHIOMETRY; THERMODYNAMICS; ANAEROBIC BACTERIUM; BIOLOGICAL MODEL; BIOMASS; CARBON CYCLE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ACETATES; AUTOTROPHIC PROCESSES; BACTERIA, ANAEROBIC; BIOMASS; CARBON CYCLE; CARBON DIOXIDE; ENERGY METABOLISM; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; THERMODYNAMICS;

EID: 84911440829     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3365     Document Type: Review

References (83)

1. Drake, H. L., Goner, A. S. & Daniel, S. L. Old acetogens, new light. Ann. NY Acad. Sci. 1125, 100-128 (2008). This elaborate review describes the history and physiology of acetogenic bacteria in detail.
2. Fontaine, F. E., Peterson, W. H., McCoy, E., Johnson, M. J. & Ritter, G. J. A new type of glucose fermentation by Clostridium thermoaceticum. J. Bacteriol. 43, 701-715 (1942).
3. Daniel, S. L., Hsu, T., Dean, S. I. & Drake, H. L. Characterization of the H2-dependent and CO-dependent chemolithotrophic potentials of the acetogens Clostridium thermoaceticum and Acetogenium kivui. J. Bacteriol. 172, 4464-4471 (1990).
4. Daniel, S. L., Keith, E. S., Yang, H. C., Lin, Y. S. & Drake, H. L. Utilization of methoxylated aromatic compounds by the acetogen Clostridium thermoaceticum - expression and specificity of the CO-dependent O-demethylating activity. Biochem. Biophys. Res. Commun. 180, 416-422 (1991).
5. Gosner, A., Daniel, S. L. & Drake, H. L. Acetogenesis coupled to the oxidation of aromatic aldehyde groups. Arch. Microbiol. 161, 126-131 (1994).
6. Drake, H. L. & Daniel, S. L. Physiology of the thermophilic acetogen Moorella thermoacetica. Res. Microbiol. 155, 869-883 (2004).
7. Seifritz, C., Frtl, J. M., Drake, H. L. & Daniel, S. L. Influence of nitrate on oxalate- and glyoxylate-dependent growth and acetogenesis by Moorella thermoacetica. Arch. Microbiol. 178, 457-464 (2002).
8. Beaty, P. S. & Ljungdahl, L. G. Thiosulfate reduction by Clostridium thermoaceticum and Clostridium thermoautothrophicum during growth on methanol. Ann. Meet. Am. Soc. Microbiol. Abstr. 1-7, 199 (1990).
9. Beaty, P. S. & Ljungdahl, L. G. Growth of Clostridium thermoaceticum on methanol, ethanol or dimethylsulfoxide. Ann. Meet. Am. Soc. Microbiol. Abstr. K-131, 236 (1991).
10. Seifritz, C., Daniel, S. L., Gosner, A. & Drake, H. L. Nitrate as a preferred electron sink for the acetogen Clostridium thermoaceticum. J. Bacteriol. 175, 8008-8013 (1993).
11. Seifritz, C., Drake, H. L. & Daniel, S. L. Nitrite as an energy-conserving electron sink for the acetogenic bacterium Moorella thermoacetica. Curr. Microbiol. 46, 329-333 (2003).
12. Ljungdahl, L. G. in Acetogenesis (eds Drake, H. L.) 63-87 (Chapman & Hall, 1994).
13. Das, A. & Ljungdahl, L. G. in Biochemistry and Physiology of Anaerobic Bacteria (eds Ljungdahl, L. G., et al.) 191-204 (Springer, 2003).
14. Muler, V. Energy conservation in acetogenic bacteria. Appl. Environ. Microbiol. 69, 6345-6353 (2003).
15. Balch, W. E., Schoberth, S., Tanner, R. S. & Wolfe, R. S. Acetobacterium, a new genus of hydrogen-oxidizing, carbon-dioxide-reducing, anaerobic bacteria. Int. J. Syst. Bact. 27, 355-361 (1977).
16. Bache, R. & Pfennig, N. Selective isolation of Acetobacterium woodii on methoxylated aromatic acids and determination of growth yields. Arch. Microbiol. 130, 255-261 (1981).
17. Eichler, B. & Schink, B. Oxidation of primary aliphatic alcohols by Acetobacterium carbinolicum sp. nov., a homoacetogenic anaerobe. Arch. Microbiol. 140, 147-152 (1984).
18. Sharak Genthner, B. R. & Bryant, M. P. Additional characteristics of one-carbon-compound utilization by Eubacterium limosum and Acetobacterium woodii. Appl. Environ. Microbiol. 53, 471-476 (1987).
19. Tschech, A. & Pfennig, N. Growth yield increase linked to caffeate reduction in Acetobacterium woodii. Arch. Microbiol. 137, 163-167 (1984).
20. Heise, R., Muler, V. & Gottschalk, G. Sodium dependence of acetate formation by the acetogenic bacterium Acetobacterium woodii. J. Bacteriol. 171, 5473-5478 (1989).
21. Muler, V. & Bowien, S. Differential effects of sodium ions on motility in the homoacetogenic bacteria Acetobacterium woodii and Sporomusa sphaeroides. Arch. Microbiol. 164, 363-369 (1995).
22. Tanner, R. S., Miller, L. M. & Yang, D. Clostridium ljungdahlii sp. nov., an acetogenic species in clostridial rRNA homology Group-I. Int. J. Syst. Bact. 43, 232-236 (1993).
23. Martin, W. F., Sousa, F. L. & Lane, N. Evolution. Energy at lifes origin. Science 344, 1092-1093 (2014).
24. Ragsdale, S. W. Pyruvate ferredoxin oxidoreductase and its radical intermediate. Chem. Rev. 103, 2333-2346 (2003).
25. Ragsdale, S. W. Enzymology of the Wood-Ljungdahl pathway of acetogenesis. Ann. NY Acad. Sci. 1125, 129-136 (2008).
26. Ljungdahl, L. G. The autotrophic pathway of acetate synthesis in acetogenic bacteria. Ann. Rev. Microbiol. 40, 415-450 (1986).
27. Wood, H. G. & Ljungdahl, L. G. in Variations in autotrophic life (eds Shively, J. M. & Barton, L. L.) (Academic press, 1991).
28. Wood, H. G., Ragsdale, S. W. & Pezacka, E. The acetyl- CoA pathway of autotrophic growth. FEMS Microbiol. Rev. 39, 345-362 (1986).
29. Thauer, R. K., Jungermann, K. & Decker, K. Energy conservation in chemotrophic anaerobic bacteria. Bact. Rev. 41, 100-180 (1977).
30. Fuchs, G. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annu. Rev. Microbiol. 65, 631-658 (2011).
31. Fuchs, G. & Stupperich, E. Acetyl CoA, a central intermediate of autotrophic CO2 fixation in Methanobacterium thermoautotrophicum. Arch. Microbiol. 127, 267-272 (1980).
32. Buckel, W. & Thauer, R. K. Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. Biochim. Biophys. Acta 1827, 94-113 (2013).
33. Poehlein, A., et al. An ancient pathway combining carbon dioxide fixation with the generation and utilization of a sodium ion gradient for ATP synthesis. PLoS ONE 7, e33439 (2012).
34. Wang, S., et al. NADP-specific electron-bifurcating [FeFe]-hydrogenase in a functional complex with formate dehydrogenase in Clostridium autoethanogenum grown on CO. J. Bacteriol. 195, 4373-4386 (2013).
35. Blakeley, R. L. & Benkovic, S. J. Folates and Pterins (John Wiley and Sons, 1984).
36. Ragsdale, S. W. & Ljungdahl, L. G. Purification and properties of NAD-dependent 5,10-methylenetetrahydrofolate dehydrogenase from Acetobacterium woodii. J. Biol. Chem. 259, 3499-3503 (1984).
37. OBrien, W. E., Brewer, J. M. & Ljungdahl, L. G. Purification and characterization of thermostable 5,10-methylenetetrahydrofolate dehydrogenase from Clostridium thermoaceticum. J. Biol. Chem. 248, 403-408 (1973).
38. Maden, B. E. Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism. Biochem. J. 350, 609-629 (2000).
39. Mock, J., Wang, S., Huang, H., Kahnt, J. & Thauer, R. K. Evidence for a hexaheteromeric methylenetetrahydrofolate reductase in Moorella thermoacetica. J. Bacteriol. 196, 3303-3314 (2014).
40. Huang, H., Wang, S., Moll, J. & Thauer, R. K. Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H2 plus CO2. J. Bacteriol. 194, 3689-3699 (2012).
41. Kike, M., et al. Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc. Natl Acad. Sci. USA 107, 13087-13092 (2010). This study provides the basis of the understanding of the industrially relevant acetogen C. ljungdahlii.
42. Muler, V., Aufurth, S. & Rahlfs, S. The Na+ cycle in Acetobacterium woodii: identification and characterization of a Na+-translocating F1F0-ATPase with a mixed oligomer of 8 and 16 kDa proteolipids. Biochim. Biophys. Acta 1505, 108-120 (2001).
43. Fritz, M., et al. An intermediate step in the evolution of ATPases: a hybrid F1F0 rotor in a bacterial Na+ F1F0 ATP synthase. FEBS J. 275, 1999-2007 (2008).
44. Brandt, K., et al. Functional production of the Na+ F1F0 ATP synthase from Acetobacterium woodii in Escherichia coli requires the native AtpI. J. Bioenerg. Biomembr. 45, 15-23 (2013).
45. Dangel, W., Schulz, H., Diekert, G., Keig, H. & Fuchs, G. Occurence of corrinoid-containing membrane proteins in anaerobic bacteria. Arch. Microbiol. 148, 52-56 (1987).
46. Biegel, E. & Muler, V. Bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase. Proc. Natl Acad. Sci. USA 107, 18138-18142 (2010).
47. Biegel, E., Schmidt, S. & Muler, V. Genetic, immunological and biochemical evidence of a Rnf complex in the acetogen Acetobacterium woodii. Environ. Microbiol. 11, 1438-1443 (2009).
48. Blaut, M. & Gottschalk, G. Protonmotive force-driven synthesis of ATP during methane formation from molecular hydrogen and formaldehyde or carbon dioxide in Methanosarcina barkeri. FEMS Microbiol. Lett. 24, 103-107 (1984).
49. Schuchmann, K. & Muler, V. A bacterial electron bifurcating hydrogenase. J. Biol. Chem. 287, 31165-31171 (2012).
50. Herrmann, G., Jayamani, E., Mai, G. & Buckel, W. Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J. Bacteriol. 190, 784-791 (2008).
51. Ragsdale, S. W., Ljungdahl, L. G. & DerVartanian, D. V. Isolation of carbon monoxide dehydrogenase from Acetobacterium woodii and comparison of its properties with those of the Clostridium thermoaceticum enzyme. J. Bacteriol. 155, 1224-1237 (1983).
52. Hess, V., Schuchmann, K. & Muler, V. The ferredoxin:NAD+ oxidoreductase (Rnf) from the acetogen Acetobacterium woodii requires Na+ and is reversibly coupled to the membrane potential. J. Biol. Chem. 288, 31496-31502 (2013).
53. Schuchmann, K. & Muler, V. Direct and reversible hydrogenation of CO2 to formate by a bacterial carbon dioxide reductase. Science 342, 1382-1385 (2013).
54. Grßer, G., Manimekalai, M. S., Mayer, F. & Muler, V. ATP synthases from archaea: the beauty of a molecular motor. Biochim. Biophys. Acta 1837, 940-952 (2014).
55. Tremblay, P. L., Zhang, T., Dar, S. A., Leang, C. & Lovley, D. R. The Rnf complex of Clostridium ljungdahlii is a proton-translocating ferredoxin:NAD+ oxidoreductase essential for autotrophic growth. mBio 4, e00406-12 (2012).
56. Sowa, Y. & Berry, R. M. Bacterial flagellar motor. Q. Rev. Biophys. 41, 103-132 (2008).
57. Mayer, F. & Muler, V. Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol. Rev. 38, 449-472 (2013).
58. Nagarajan, H., et al. Characterizing acetogenic metabolism using a genome-scale metabolic reconstruction of Clostridium ljungdahlii. Microb. Cell. Fact. 12, 118 (2013).
59. Schut, G. J. & Adams, M. W. The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J. Bacteriol. 191, 4451-4457 (2009).
60. Wang, S., Huang, H., Kahnt, J. & Thauer, R. K. A reversible electron-bifurcating ferredoxin- and NAD-dependent [FeFe]-hydrogenase (HydABC) in Moorella thermoacetica. J. Bacteriol. 195, 1267-1275 (2013).
61. Wang, S., Huang, H., Moll, J. & Thauer, R. K. NADP+ reduction with reduced ferredoxin and NADP+ reduction with NADH are coupled via an electron bifurcating enzyme complex in Clostridium kluyveri. J. Bacteriol. 192, 5115-5123 (2010).
62. Pierce, E., et al. The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ. Microbiol. 10, 2550-2573 (2008).
63. Hugenholtz, J. & Ljungdahl, L. G. Metabolism and energy generation in homoacetogenic clostridia. FEMS Microbiol. Rev. 87, 383-389 (1990).
64. Hedderich, R. & Forzi, L. Energy-converting [NiFe] hydrogenases: more than just H2 activation. J. Mol. Microbiol. Biotechnol. 10, 92-104 (2005).
65. Kukel, A., Vorholt, J. A., Thauer, R. K. & Hedderich, R. An Escherichia coli hydrogenase-3-type hydrogenase in methanogenic archaea. Eur. J. Biochem. 252, 467-476 (1998).
66. Fox, J. D., He, Y., Shelver, D., Roberts, G. P. & Ludden, P. W. Characterization of the region encoding the CO-induced hydrogenase of Rhodospirillum rubrum. J. Bacteriol. 178, 6200-6208 (1996).
67. Sauter, M., Bohm, R. & Bock, A. Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol. Microbiol. 6, 1523-1532 (1992).
68. Welte, C., Kratzer, C. & Deppenmeier, U. Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei. FEBS J. 277, 3396-3403 (2010).
69. Welte, C. & Deppenmeier, U. Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens. Biochim. Biophys. Acta 1837, 1130-1147 (2014).
70. Yamamoto, I., Saiki, T., Liu, S. M. & Ljungdahl, L. G. Purification and properties of NADP-dependent formate dehydrogenase from Clostridium thermoaceticum, a tungsten-selenium-iron protein. J. Biol. Chem. 258, 1826-1832 (1983).
71. Ljungdahl, L. G. & Andreesen, J. R. Tungsten, a component of active formate dehydrogenase from Clostridium thermoacetium. FEBS Lett. 54, 279-282 (1975).
72. Frostl, J. M., Seifritz, C. & Drake, H. L. Effect of nitrate on the autotrophic metabolism of the acetogens Clostridium thermoautotrophicum and Clostridium thermoaceticum. J. Bacteriol. 178, 4597-4603 (1996).
73. Arendsen, A. F., Soliman, M. Q. & Ragsdale, S. W. Nitrate-dependent regulation of acetate biosynthesis and nitrate respiration by Clostridium thermoaceticum. J. Bacteriol. 181, 1489-1495 (1999).
74. Ragsdale, S. W., Clark, J. E., Ljungdahl, L. G., Lundie, L. L. & Drake, H. L. Properties of purified carbon monoxide dehydrogenase from Clostridium thermoaceticum, a nickel, iron-sulfur protein. J. Biol. Chem. 258, 2364-2369 (1983).
75. Oehler, D., et al. Genome-guided analysis of physiological and morphological traits of the fermentative acetate oxidizer Thermacetogenium phaeum. BMC Genomics 13, 723 (2012).
76. Banerjee, A., Leang, C., Ueki, T., Nevin, K. P. & Lovley, D. R. Lactose-inducible system for metabolic engineering of Clostridium ljungdahlii. Appl. Environ. Microbiol. 80, 2410-2416 (2014).
77. Leang, C., Ueki, T., Nevin, K. P. & Lovley, D. R. A genetic system for Clostridium ljungdahlii: a chassis for autotrophic production of biocommodities and a model homoacetogen. Appl. Environ. Microbiol. 79, 1102-1109 (2013).
78. Ragsdale, S. W. & Pierce, E. Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim. Biophys. Acta 1784, 1873-1898 (2008).
79. Bennett, B. D., et al. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nature Chem. Biol. 5, 593-599 (2009).
80. Bar-Even, A. Does acetogenesis really require especially low reduction potential? Biochim. Biophys. Acta 1827, 395-400 (2013).
81. Bender, G. & Ragsdale, C. W. Evidence that ferredoxin interfaces with an internal redox shuttle in Acetyl-CoA synthase during reductive activation and catalysis. Biochemistry 50, 276-286 (2011).
82. Li, F., et al. Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl- CoA dehydrogenase/Etf complex from Clostridium kluyveri. J. Bacteriol. 190, 843-850 (2008).
83. Chowdhury, N. P., et al. Studies on the mechanism of electron bifurcation catalyzed by electron transferring flavoprotein (Etf) and butyryl-CoA dehydrogenase (Bcd) of Acidaminococcus fermentans. J. Biol. Chem. 289, 5145-5157 (2014).