A genome-guided analysis of energy conservation in the thermophilic, cytochrome-free acetogenic bacterium Thermoanaerobacter kivui

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Hess, Verena ^a   Poehlein, Anja ^b   Weghoff, Marie Charlotte ^a   Daniel, Rolf ^b   Müller, Volker ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Acetogen; Ech; Energy conservation; Genome sequence; H+ transport; Thermoanaerobacter kivui

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ENOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCOSE 6 PHOSPHATE ISOMERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEXOKINASE; ISOMERASE; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE MUTASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; TRIOSE P ISOMERASE; UNCLASSIFIED DRUG; ACETIC ACID DERIVATIVE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ACETOBACTERIUM; ACETOBACTERIUM WOODII; AMINO ACID SUBSTITUTION; ARTICLE; AUTOTROPHY; BACTERIAL GENE; BINDING SITE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENERGY CONSERVATION; ENZYME ACTIVITY; FDHD GENE; FDHF GENE; GENE CLUSTER; GENE SEQUENCE; GENOME ANALYSIS; HYCB3 GENE; HYCB4 GENE; MOORELLA THERMOACETICA; NONHUMAN; NUCLEOTIDE SEQUENCE; THERMOANAEROBACTER; THERMOANAEROBACTER BROCKII FINII; THERMOANAEROBACTER KIVUI; THERMOANAEROBACTER MATHRANII MATHRANII; THERMOANAEROBACTER WIEGELII; AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; DNA SEQUENCE; ENERGY METABOLISM; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS;

ACETOBACTERIUM WOODII; BACTERIA (MICROORGANISMS); THERMOANAEROBACTER KIVUI;

ACETATES; AMINO ACID SEQUENCE; AUTOTROPHIC PROCESSES; CELL MEMBRANE; ELECTRON TRANSPORT; ENERGY METABOLISM; GENOMICS; MOLECULAR SEQUENCE DATA; PROTON-TRANSLOCATING ATPASES; SEQUENCE ANALYSIS, DNA; THERMOANAEROBACTER;

EID: 84924328742     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1139     Document Type: Article

References (78)

1. Drake HL, Gößner AS, Daniel SL: Old acetogens, new light. Ann N Y Acad Sci 2008, 1125:100-128. 10.1196/annals.1419.016
2. Müller V, Frerichs J: Acetogenic bacteria. In eLS. Edited by: Battista J. Chichester: John Wiley & Sons Ltd; 2013. [doi:10.1002/9780470015902.a0020086.pub2]
3. Ljungdahl LG: The acetyl-CoA pathway and the chemiosmotic generation of ATP during acetogenesis. In Acetogenesis. Edited by: Drake HL. New York: Chapman & Hall; 1994:63-87.
4. Ragsdale SW: Enzymology of the Wood-Ljungdahl pathway of acetogenesis. Ann N Y Acad Sci 2008, 1125:129-136. 10.1196/annals.1419.015
5. Pezacka E, Wood HG: Role of carbon monoxide dehydrogenase in the autotrophic pathway used by acetogenic bacteria. Proc Natl Acad Sci U S A 1984, 81:6261-6265. 10.1073/pnas.81.20.6261
6. Raybuck SA, Bastian NR, Orme-Johnson WH, Walsh CT: Kinetic characterization of the carbon monoxide-acetyl-CoA (carbonyl group) exchange activity of the acetyl-CoA synthesizing CO dehydrogenase from Clostridium thermoaceticum . Biochemistry 1988, 27:7698-7702. 10.1021/bi00420a019
7. Seravalli J, Kumar M, Lu WP, Ragsdale SW: Mechanism of carbon monoxide oxidation by the carbon monoxide dehydrogenase/acetyl-CoA synthase from Clostridium thermoaceticum: Kinetic characterization of the intermediates. Biochemistry 1997, 36:11241-11251. 10.1021/bi970590m
8. Himes RH, Harmony JA: Formyltetrahydrofolate synthetase. Crc Cr Rev Bioch Mol 1973, 1:501-535. 10.3109/10409237309105441
9. Lovell CR, Przybyla A, Ljungdahl LG: Cloning and expression in Escherichia coli of the Clostridium thermoaceticum gene encoding thermostable formyltetrahydrofolate synthetase. Arch Microbiol 1988, 149:280-285. 10.1007/BF00411642
10. Ragsdale SW, Ljungdahl LG, DerVartanian DV: EPR evidence for nickel-substrate interaction in carbon monoxide dehydrogenase from Clostridium thermoaceticum . Biochem Biophys Res Commun 1982, 108:658-663. 10.1016/0006-291X(82)90880-4
11. Ragsdale SW, Ljungdahl LG, DerVartanian DV: Isolation of carbon monoxide dehydrogenase from Acetobacterium woodii and comparison of its properties with those of the Clostridium thermoaceticum enzyme. J Bacteriol 1983, 155:1224-1237.
12. Ragsdale SW, Wood HG: Acetate biosynthesis by acetogenic bacteria. Evidence that carbon monoxide dehydrogenase is the condensing enzyme that catalyzes the final steps in the synthesis. J Biol Chem 1985, 260:3970-3977.
13. Schaupp A, Ljungdahl LG: Purification and properties of acetate kinase from Clostridium thermoaceticum . Arch Microbiol 1974, 100:121-129. 10.1007/BF00446312
14. 2 fixation in Acetobacterium woodii . Arch Microbiol 1982, 133:66-74. 10.1007/BF00943772
15. Biegel E, Schmidt S, González JM, Müller V: Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell Mol Life Sci 2011, 68:613-634. 10.1007/s00018-010-0555-8
16. + oxidoreductase. Proc Natl Acad Sci U S A 2010, 107:18138-18142. 10.1073/pnas.1010318107
17. Heise R, Reidlinger J, Müller V, Gottschalk G: A sodium-stimulated ATP synthase in the acetogenic bacterium Acetobacterium woodii . FEBS Lett 1991, 295:119-122. 10.1016/0014-5793(91)81400-3
18. O -ATPase with a mixed oligomer of 8 and 16 kDa proteolipids. Biochim Biophys Acta 2001, 1505:108-120. 10.1016/S0005-2728(00)00281-4
19. Schuchmann K, Müller V: Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 2014, 12:809-821. 10.1038/nrmicro3365
20. Fröstl JM, Seifritz C, Drake HL: Effect of nitrate on the autotrophic metabolism of the acetogens Clostridium thermoautotrophicum and Clostridium thermoaceticum . J Bacteriol 1996, 178:4597-4603.
21. Seifritz C, Daniel SL, Gössner A, Drake HL: Nitrate as a preferred electron sink for the acetogen Clostridium thermoaceticum . J Bacteriol 1993, 175:8008-8013.
22. Dilling S, Imkamp F, Schmidt S, Müller V: Regulation of caffeate respiration in the acetogenic bacterium Acetobacterium woodii . Appl Environ Microbiol 2007, 73:3630-3636. 10.1128/AEM.02060-06
23. 2 and aromatic acrylate groups as competing electron accepters. Microbiology-Uk 1996, 142:1983-1988. 10.1099/13500872-142-8-1983
24. Gössner A, Daniel SL, Drake HL: Acetogenesis coupled to the oxidation of aromatic aldehyde groups. Arch Microbiol 1994, 161:126-131. 10.1007/BF00276472
25. Matthies C, Freiberger A, Drake HL: Fumarate dissimilation and differential reductant flow by Clostridium formicoaceticum and Clostridium aceticum . Arch Microbiol 1993, 160:273-278. 10.1007/BF00292076
26. Tanner RS, Miller LM, Yang D: Clostridium ljungdahlii sp. nov., an acetogenic species in clostridial rRNA homology Group-I. Int J Syst Bact 1993, 43:232-236. 10.1099/00207713-43-2-232
27. Liou JS, Balkwill DL, Drake GR, Tanner RS: Clostridium carboxidivorans sp. nov., a solvent-producing clostridium isolated from an agricultural settling lagoon, and reclassification of the acetogen Clostridium scatologenes strain SL1 as Clostridium drakei sp. nov. Int J Syst Evol Microbiol 2005, 55:2085-2091. 10.1099/ijs.0.63482-0
28. Schiel-Bengelsdorf B, Dürre P: Pathway engineering and synthetic biology using acetogens. FEBS Lett 2012, 586:2191-2198. 10.1016/j.febslet.2012.04.043
29. Köpke M, Mihalcea C, Liew F, Tizard JH, Ali MS, Conolly JJ, Al-Sinawi B, Simpson SD: 2,3-butanediol production by acetogenic bacteria, an alternative route to chemical synthesis, using industrial waste gas. Appl Environ Microbiol 2011, 77:5467-5475. 10.1128/AEM.00355-11
30. Pierce E, Xie G, Barabote RD, Saunders E, Han CS, Detter JC, Richardson P, Brettin TS, Das A, Ljungdahl LG, Ragsdale SW: The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum ). Environ Microbiol 2008, 10:2550-2573. 10.1111/j.1462-2920.2008.01679.x
31. Mock J, Wang S, Huang H, Kahnt J, Thauer RK: Evidence for a hexaheteromeric methylenetetrahydrofolate reductase in Moorella thermoacetica . J Bacteriol 2014, 196:3303-3314. 10.1128/JB.01839-14
32. 2 . J Bacteriol 2012, 194:3689-3699. 10.1128/JB.00385-12
33. Leigh JA, Mayer F, Wolfe RS: Acetogenium kivui, a new thermophilic hydrogen-oxidizing, acetogenic bacterium. Arch Microbiol 1981, 129:275-280. 10.1007/BF00414697
34. 2 -dependent and CO-dependent chemolithotrophic potentials of the acetogens Clostridium thermoaceticum and Acetogenium kivui . J Bacteriol 1990, 172:4464-4471.
35. Yang H, Drake HL: Differential effects of sodium on hydrogen- and glucose-dependent growth of the acetogenic bacterium Acetogenium kivui . Appl Environ Microbiol 1990, 56:81-86.
36. Bradford MM: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of proteine-dye-binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3
37. + and is reversibly coupled to the membrane potential. J Biol Chem 2013, 288:31496-31502. 10.1074/jbc.M113.510255
38. Schönheit P, Wäscher C, Thauer RK: A rapid procedure for the purification of ferredoxin from clostridia using polyethylenimine. FEBS Lett 1978, 89:219-222. 10.1016/0014-5793(78)80221-X
39. Murray MG, Thompson WF: Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 1980, 8:4321-4325. 10.1093/nar/8.19.4321
40. Wilson K: Preparation of genomic DNA from bacteria. In Current Protocols in Molecular Biology. Edited by: Ausubel FM. Hoboken: John Wiley & Sons, Inc; 2001:56:2.4.1.-2.4.5.
41. Chevreux B: MIRA: an automated genome and EST assembler. Heidelberg: Ruprecht-Karls University; 2005.
42. Darling AE, Mau B, Perna NT: progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010, 5:e11147. 10.1371/journal.pone.0011147
43. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Pillay M, Ratner A, Huang J, Woyke T, Huntemann M, Anderson I, Billis K, Varghese N, Mavromatis K, Pati A, Ivanova NN, Kyrpides NC: IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res 2014, 42:D560-D567. 10.1093/nar/gkt963
44. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyprides NC: IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res 2012, 40:D115-D122. 10.1093/nar/gkr1044
45. Tettelin H, Radune D, Kasif S, Khouri H, Salzberg SL: Optimized multiplex PCR: efficiently closing a whole-genome shotgun sequencing project. Genomics 1999, 62:500-507. 10.1006/geno.1999.6048
46. Staden R, Beal KF, Bonfield JK: The Staden package, 1998. Methods Mol Biol 2000, 132:115-130.
47. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ: Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010, 11:119. 10.1186/1471-2105-11-119
48. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW: RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007, 35:3100-3108. 10.1093/nar/gkm160
49. Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964. 10.1093/nar/25.5.0955
50. Zdobnov EM, Apweiler R: InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17:847-848. 10.1093/bioinformatics/17.9.847
51. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS: PHAST: a fast phage search tool. Nucleic Acids Res 2011, 39:W347-W352. 10.1093/nar/gkr485
52. Schmidt K, Liaaen Jensen S, Schlegel HG: Die Carotinoide der Thiorhodaceae. I Okenon als Hauptcarotinoid von Chromatium okenii Perty. Arch Mikrobiol 1963, 46:117-126. 10.1007/BF00408204
53. Horvath P, Barrangou R: CRISPR/Cas, the immune system of bacteria and archaea. Science 2010, 327:167-170. 10.1126/science.1179555
54. Haft DH, Selengut J, Mongodin EF, Nelson KE: A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 2005, 1:e60. 10.1371/journal.pcbi.0010060
55. Westra ER, Brouns SJ: The rise and fall of CRISPRs-dynamics of spacer acquisition and loss. Mol Microbiol 2012, 85:1021-1025. 10.1111/j.1365-2958.2012.08170.x
56. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, van der Oost J, Koonin EV: Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 2011, 9:467-477. 10.1038/nrmicro2577
57. Poehlein A, Schmidt S, Kaster A-K, Goenrich M, Vollmers J, Thürmer A, Bertsch J, Schuchmann K, Voigt B, Hecker M, Daniel R, Thauer RK, Gottschalk G, Müller V: An ancient pathway combining carbon dioxide fixation with the generation and utilization of a sodium ion gradient for ATP synthesis. PLoS One 2012, 7:e33439. 10.1371/journal.pone.0033439
58. 2 to formate by a bacterial carbon dioxide reductase. Science 2013, 342:1382-1385. 10.1126/science.1244758
59. Li LF, Ljungdahl L, Wood HG: Properties of nicotinamide adenine dinucleotide phosphate-dependent formate dehydrogenase from Clostridium thermoaceticum . J Bacteriol 1966, 92:405-412.
60. Schuchmann K, Müller V: A bacterial electron bifurcating hydrogenase. J Biol Chem 2012, 287:31165-31171. 10.1074/jbc.M112.395038
61. Schut GJ, Adams MW: The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 2009, 191:4451-4457. 10.1128/JB.01582-08
62. Wang S, Huang H, Kahnt J, Thauer RK: A reversible electron-bifurcating ferredoxin- and NAD-dependent [FeFe]-hydrogenase (HydABC) in Moorella thermoacetica . J Bacteriol 2013, 195:1267-1275. 10.1128/JB.02158-12
63. Müller V, Grüber G: ATP synthases: structure, function and evolution of unique energy converters. Cell Mol Life Sci 2003, 60:474-494. 10.1007/s000180300040
64. O ATP synthase from Acetobacterium woodii in Escherichia coli requires the native AtpI. J Bioenerg Biomembr 2013, 45:15-23. 10.1007/s10863-012-9474-8
65. O -ATPase operon from Acetobacterium woodii . Operon structure and presence of multiple copies of atpE which encode proteolipids of 8- and 18-kDa. J Biol Chem 1999, 274:33999-34004. 10.1074/jbc.274.48.33999
66. + -dependent F-ATP synthases. J Mol Biol 2009, 391:498-507. 10.1016/j.jmb.2009.05.082
67. Hedderich R: Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr 2004, 36:65-75.
68. Welte C, Krätzer C, Deppenmeier U: Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei . FEBS J 2010, 277:3396-3403. 10.1111/j.1742-4658.2010.07744.x
69. Meuer J, Bartoschek S, Koch J, Künkel A, Hedderich R: Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri . Eur J Biochem 1999, 265:325-335. 10.1046/j.1432-1327.1999.00738.x
70. Welte C, Deppenmeier U: Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens. Biochim Biophys Acta 2013, 1837:1130-1147.
71. 2 activation. J Mol Microbiol Biotechnol 2005, 10:92-104. 10.1159/000091557
72. 1 metabolism. Biochem J 2000, 350:609-629. 10.1042/0264-6021:3500609
73. Thauer RK, Jungermann K, Decker K: Energy conservation in chemotrophic anaerobic bacteria. Bact Rev 1977, 41:100-180.
74. Gottwald M, Andreesen JR, LeGall J, Ljungdahl LG: Presence of cytochrome and menaquinone in Clostridium formicoaceticum and Clostridium thermoaceticum . J Bacteriol 1975, 122:325-328.
75. Hugenholtz J, Ivey DM, Ljungdahl LG: Carbon monoxide-driven electron transport in Clostridium thermoautotrophicum membranes. J Bacteriol 1987, 169:5845-5847.
76. Hugenholtz J, Ljungdahl LG: Electron transport and electrochemical proton gradient in membrane vesicles of Clostridium thermoaceticum . J Bacteriol 1989, 171:2873-2875.
77. Hugenholtz J, Ljungdahl LG: Amino acid transport in membrane vesicles of Clostridium thermoautotrophicum . FEMS Microbiol Lett 1990, 69:117-122. 10.1111/j.1574-6968.1990.tb04186.x
78. Martin WF: Hydrogen, metals, bifurcating electrons, and proton gradients: the early evolution of biological energy conservation. FEBS Lett 2012, 586:485-493. 10.1016/j.febslet.2011.09.031