Identification of key components in the energy metabolism of the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus by transcriptome analyses

Frontiers in Microbiology

Volumn 5, Issue MAR, 2014, Pages

  Hocking, William P ^a   Stokke, Runar ^a   Roalkvam, Irene ^a   Steen, Ida H ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

Archaeoglobus fulgidus; Dissimilatory sulfate reduction; Heterodisulfide reductase; Hydrogenase; Lactate dehydrogenase

Indexed keywords

ACETYL COENZYME A; HYDROGENASE; LACTATE DEHYDROGENASE; SULFATE; THIOSULFATE; TRANSCRIPTOME;

ARCHAEOGLOBUS FULGIDUS; ARTICLE; CELL MOTILITY; ENERGY CONSERVATION; ENERGY METABOLISM; GENE LOCUS; GROWTH CURVE; HYPERTHERMOPHILIC ARCHAEON; LITHOTROPH; MEMBRANE TRANSPORT; MICROARRAY ANALYSIS; NONHUMAN; SIGNAL TRANSDUCTION; SULFATE REDUCING ARCHAEON; UPREGULATION;

EID: 84897931364     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00095     Document Type: Article

References (114)

1. Alex, L. A., Reeve, J. N., Orme-Johnson, W. H., and Walsh, C. T. (1990). Cloning, sequence determination, and expression of the genes encoding the subunits of the nickel-containing 8-hydroxy-5-deazaflavin reducing hydrogenase from Methanobacterium thermoautotrophicum ΔH. Biochemistry 29, 7237-7244. doi: 10.1021/bi00483a011.
2. Auernik, K. S., and Kelly, R. M. (2010). Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by transcriptomic analysis of heterotrophic, autotrophic, and mixotrophic growth. Appl. Environ. Microbiol. 76, 931-935. doi: 10.1128/AEM.01336-09.
3. Badziong, W., and Thauer, R. (1978). Growth yields and growth rates of Desulfovibrio vulgaris (Marburg) growing on hydrogen plus sulfate and hydrogen plus thiosulfate as the sole energy sources. Arch. Microbiol. 117, 209-214. doi: 10.1007/BF00402310.
4. Banerjee, R., and Ragsdale, S. W. (2003). The many faces of vitamin B12: catalysis by cobalamin-dependent enzymes. Annu. Rev. Microbiol. 72, 209-247. doi: 10.1146/annurev.biochem.72.121801.161828.
5. 2 dehydrogenase from Methanosarcina mazei is a Redox-driven proton pump closely related to NADH dehydrogenases. J. Biol. Chem. 275, 17968-17973. doi: 10.1074/jbc.M000650200.
6. Berg, I. A., Kockelkorn, D., Buckel, W., and Fuchs, G. (2007). A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318, 1782-1786. doi: 10.1126/science.1149976.
7. Biegel, E., Schmidt, S., González, J. M., and Müller, V. (2011). Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell. Mol. Life Sci. 68, 613-634. doi: 10.1007/s00018-010-0555-8.
8. Bolstad, B. M., Irizarry, R. A., Åstrand, M., and Speed, T. P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193. doi: 10.1093/bioinformatics/19.2.185.
9. 2 with the phosphorylation of ADP in acetate-grown Methanosarcina barkeri. Eur. J. Biochem. 159, 393-398. doi: 10.1111/j.1432-1033.1986.tb09881.x.
10. 2 in methanogenic bacteria. Eur. J. Biochem. 168, 407-412. doi: 10.1111/j.1432-1033.1987.tb13434.x.
11. Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P. (2008). Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245-252. doi: 10.1038/nrmicro1852.
12. 2: quinone oxidoreductase of Archaeoglobus fulgidus. Eur. J. Biochem. 267, 5810-5814. doi: 10.1046/j.1432-1327.2000.01657.x.
13. Buckel, W., and Thauer, R. K. (2013). Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. Biochim. Biophys. Acta 1827, 94-113. doi: 10.1016/j.bbabio.2012.07.002.
14. Callaghan, A. V., Morris, B. E. L., Pereira, I. A. C., McInerney, M. J., Austin, R. N., Groves, J. T., et al. (2012). The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation. Environ. Microbiol. 14, 101-113. doi: 10.1111/j.1462-2920.2011.02516.x.
15. Chai, Y., Kolter, R., and Losick, R. (2009). A widely conserved gene cluster required for lactate utilization in Bacillus subtilis and its involvement in biofilm formation. J. Bacteriol. 191, 2423-2430. doi: 10.1128/JB.01464-08.
16. Chance, B., and Hollunger, G. (1960). Energy-linked reduction of mitochondrial pyridine nucleotide. Nature 185, 666-672. doi: 10.1038/185666a0.
17. Coulthurst, S. J., Dawson, A., Hunter, W. N., and Sargent, F. (2012). Conserved signal peptide recognition systems across the prokaryotic domains. Biochemistry 51, 1678-1686. doi: 10.1021/bi201852d.
18. Cypionka, H. (1987). Uptake of sulfate, sulfite and thiosulfate by proton-anion symport in Desulfovibrio desulfuricans. Arch. Microbiol. 148, 144-149. doi: 10.1007/BF00425363.
19. Dai, Y., Reed, D. W., Millstein, J. H., Hartzell, P. L., Grahame, D. A., and DeMoll, E. (1998). Acetyl-CoA decarbonylase/synthase complex from Archaeoglobus fulgidus. Arch. Microbiol. 169, 525-529. doi: 10.1007/s002030050606.
20. Deppenmeier, U., Blaut, M., Schmidt, B., and Gottschalk, G. (1992). Purification and properties of a F420-nonreactive, membrane-bound hydrogenase from Methanosarcina strain Gö1. Arch. Microbiol. 157, 505-511. doi: 10.1007/BF00276770.
21. Despalins, A., Marsit, S., and Oberto, J. (2011). Absynte: a web tool to analyze the evolution of orthologous archaeal and bacterial gene clusters. Bioinformatics 27, 2905-2906. doi: 10.1093/bioinformatics/btr473.
22. Elbehti, A., Brasseur, G., and Lemesle-Meunier, D. (2000). First evidence for existence of an uphill electron transfer through the bc1 and NADH-Q oxidoreductase complexes of the acidophilic obligate chemolithotrophic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans. J. Bacteriol. 182, 3602-3606. doi: 10.1128/JB.182.12.3602-3606.2000.
23. Estelmann, S., Ramos-vera, W. H., Gad'on, N., Huber, H., Berg, I. A., and Fuchs, G. (2011). Carbon dioxide oxidation in "Archaeoglobus lithotrophicus": are there multiple autotrophic pathways? FEMS Microbiol. Lett. 319, 65-72. doi: 10.1111/j.1574-6968.2011.02268.x.
24. Fellenberg, K., Hauser, N. C., Brors, B., Neutzner, A., Hoheisel, J. D., and Vingron, M. (2001). Correspondence analysis applied to microarray data. Proc. Natl. Acad. Sci. U.S.A. 98, 10781-10786. doi: 10.1073/pnas.181597298.
25. Fiévet, A., My, L., Cascales, E., Ansaldi, M., Pauleta, S. R., Moura, I., et al. (2011). The anaerobe-specific orange protein complex of Desulfovibrio vulgaris Hildenborough is encoded by two divergent operons coregulated by s54 and a cognate transcriptional regulator. J. Bacteriol. 193, 3207-3219. doi: 10.1128/JB.00044-11.
26. Fuchs, G. (2011). Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annu. Rev. Microbiol. 65, 631-658. doi: 10.1146/annurev-micro-090110-102801.
27. Grein, F., Pereira, I. A. C., and Dahl, C. (2010). Biochemical characterization of individual components of the Allochromatium vinosum DsrMKJOP transmembrane complex aids understanding of complex function in vivo. J. Bacteriol. 192, 6369-6377. doi: 10.1128/JB.00849-10.
28. Grein, F., Ramos, A. R., Venceslau, S. S., and Pereira, I. A. C. (2013). Unifying concepts in anaerobic respiration: insights from dissimilatory sulfur metabolism. Biochim. Biophys. Acta 1827, 145-160. doi: 10.1016/j.bbabio.2012.09.001.
29. Guy, L., and Ettema, T. J. G. (2011). The archaeal "TACK" superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580-587. doi: 10.1016/j.tim.2011.09.002.
30. Hale, C. R., Zhao, P., Olson, S., Duff, M. O., Graveley, B. R., Wells, L., et al. (2009). RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139, 945-956. doi: 10.1016/j.cell.2009.07.040.
31. Hartzell, P., and Reed, D. W. (2006). "The genus Archaeoglobus," in The Prokaryotes Volume 3: Archaea. Bacteria: Firmicutes, Actinomycetes, eds M. Dworkin, S. Falkow, E. Rosenberg, K. Schleifer, and E. Stackebrandt (New York, NY: Springer), 82-100.
32. Hedderich, R. (2004). Energy-converting [NiFe] hydrogenases from Archaea and extremophiles: ancestors of complex I. J. Bioenerg. Biomembr. 36, 65-75. doi: 10.1023/B:JOBB.0000019599.43969.33.
33. Henstra, A. M., Dijkema, C., and Stams, A. J. M. (2007). Archaeoglobus fulgidus couples CO oxidation to sulfate reduction and acetogenesis with transient formate accumulation. Environ. Microbiol. 9, 1836-1841. doi: 10.1111/j.1462-2920.2007.01306.x.
34. Hollenstein, K., Frei, D. C., and Locher, K. P. (2007). Structure of an ABC transporter in complex with its binding protein. Nature 446, 213-216. doi: 10.1038/nature05626.
35. 2. J. Bacteriol. 194, 3689-3699. doi: 10.1128/JB.00385-12.
36. 2: heterodisulfide oxidoreductase from Methanosarcina mazei Gö1: identification of two proton-translocating segments. J. Bacteriol. 181, 4076-4080.
37. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., et al. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264. doi: 10.1093/biostatistics/4.2.249.
38. Kaster, A., Moll, J., Parey, K., and Thauer, R. K. (2011). Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. Proc. Natl. Acad. Sci. U.S.A. 108, 2981-2986. doi: 10.1073/pnas.1016761108.
39. Keller, K. L., and Wall, J. D. (2011). Genetics and molecular biology of the electron flow for sulfate respiration in Desulfovibrio. Front. Microbiol. 2:135. doi: 10.3389/fmicb.2011.00135.
40. Khelifi, N., Grossi, V., Hamdi, M., Dolla, A., Tholozan, J.-L., Ollivier, B., et al. (2010). Anaerobic oxidation of fatty acids and alkenes by the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus. Appl. Environ. Microbiol. 76, 3057-3060. doi: 10.1128/AEM.02810-09.
41. Klein, M., Friedrich, M., Roger, A. J., Hugenholtz, P., Fishbain, S., Abicht, H., et al. (2001). Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J. Bacteriol. 183, 6028-6035. doi: 10.1128/JB.183.20.6028-6035.2001.
42. Klenk, H. P., Clayton, R. A., Tomb, J. F., White, O., Nelson, K. E., Ketchum, K. A., et al. (1997). The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390, 364-370. doi: 10.1038/37052.
43. Kulkarni, G., Kridelbaugh, D. M., Guss, A. M., and Metcalf, W. W. (2009). Hydrogen is a preferred intermediate in the energy-conserving electron transport chain of Methanosarcina barkeri. Proc. Natl. Acad. Sci. U.S.A. 106, 15915-15920. doi: 10.1073/pnas.0905914106.
44. 2: quinone oxidoreductase from Archaeoglobus fulgidus characterization of a membrane-bound multisubunit complex containing FAD and iron-sulfur clusters. Eur. J. Biochem. 223, 503-511. doi: 10.1111/j.1432-1033.1994.tb19019.x.
45. Kunow, J., Schwörer, B., Stetter, K. O., and Thauer, R. K. (1993). A F420-dependent NADP reductase in the extremely thermophilic sulfate-reducing Archaeoglobus fulgidus. Arch. Microbiol. 160, 199-205. doi: 10.1007/BF00249125.
46. Lenz, O., Bernhard, M., Buhrke, T., Schwartz, E., and Friedrich, B. (2002). The hydrogen-sensing apparatus in Ralstonia eutropha. J. Mol. Microbiol. Biotechnol. 4, 255-262.
47. Li, F., Hinderberger, J., Seedorf, H., Zhang, J., Buckel, W., and Thauer, R. K. (2008). 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. doi: 10.1128/JB.01417-07.
48. Lie, T. J., Costa, K. C., Lupa, B., Korpole, S., Whitman, W. B., and Leigh, J. A. (2012). Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis. Proc. Natl. Acad. Sci. U.S.A. 109, 15473-15478. doi: 10.1073/pnas.1208779109.
49. Liebensteiner, M. G., Pinkse, M. W. H., Schaap, P. J., Stams, A. J. M., and Lomans, B. P. (2013). Archaeal (Per)Chlorate reduction at high temperature: an interplay of biotic and abiotic reactions. Science. 340, 85-87. doi: 10.1126/science.1233957.
50. Mander, G. J., Duin, E. C., Linder, D., Stetter, K. O., and Hedderich, R. (2002). Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea. Eur. J. Biochem. 269, 1895-1904. doi: 10.1046/j.1432-1033.2002.02839.x.
51. Mander, G. J., Pierik, A. J., Huber, H., and Hedderich, R. (2004). Two distinct heterodisulfide reductase-like enzymes in the sulfate-reducing archaeon Archaeoglobus profundus. Eur. J. Biochem. 271, 1106-1116. doi: 10.1111/j.1432-1033.2004.04013.x.
52. Mander, G. J., Weiss, M. S., Hedderich, R., Kahnt, J., Ermler, U., and Warkentin, E. (2005). X-ray structure of the gamma-subunit of a dissimilatory sulfite reductase: fixed and flexible C-terminal arms. FEBS Lett. 579, 4600-4604. doi: 10.1016/j.febslet.2005.07.029.
53. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., et al. (2011). CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229. doi: 10.1093/nar/gkq1189.
54. Matschiavelli, N., Oelgeschläger, E., Cocchiararo, B., Finke, J., and Rother, M. (2012). Function and regulation of isoforms of carbon monoxide dehydrogenase/acetyl coenzyme A synthase in Methanosarcina acetivorans. J. Bacteriol. 194, 5377-5387. doi: 10.1128/JB.00881-12.
55. Meuer, J., Bartoschek, S., Koch, J., Künkel, A., and Hedderich, R. (1999). Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri. Eur. J. Biochem. 265, 325-335. doi: 10.1046/j.1432-1327.1999.00738.x.
56. 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. doi: 10.1128/JB.01959-12.
57. Meyer, B., and Kuever, J. (2007). Phylogeny of the alpha and beta subunits of the dissimilatory adenosine-5'-phosphosulfate (APS) reductase from sulfate-reducing prokaryotes-origin and evolution of the dissimilatory sulfate-reduction pathway. Microbiology 153, 2026-2044. doi: 10.1099/mic.0.2006/003152-0.
58. Möller-Zinkhan, D., Börner, G., and Thauer, R. K. (1989). Function of methanofuran, tetrahydromethanopterin, and coenzyme F420 in Archaeoglobus fulgidus. Arch. Microbiol. 152, 362-368. doi: 10.1007/BF00425174.
59. 2 by Archaeoglobus fulgidus via the carbon monoxide dehydrogenase pathway: demonstration of the acetyl-CoA carbon-carbon cleavage reaction in cell extracts. Arch. Microbiol. 153, 215-218. doi: 10.1007/BF00249070.
60. Moon, Y.-J., Kwon, J., Yun, S.-H., Lim, H. L., Kim, M.-S., Kang, S. G., et al. (2012). Proteome analyses of hydrogen-producing hyperthermophilic archaeon Thermococcus onnurineus NA1 in different one-carbon substrate culture conditions. Mol. Cell. Proteomics 11:M111.015420. doi: 10.1074/mcp.M111.015420.
61. Moparthi, V. K., and Hägerhäll, C. (2011). The evolution of respiratory chain Complex I from a smaller last common ancestor consisting of 11 protein subunits. J. Mol. Evol. 72, 484-497. doi: 10.1007/s00239-011-9447-2.
62. Nimblegen systems. (2007). NimbleChip Arrays User's Guide. Available online at: http://www.ebi.ac.uk/microarray-srv/manufacturer/NimbleChip_Expression_User_Guide_16Jan2007.pdf.
63. Noll, K. M., and Barber, T. S. (1988). Vitamin contents of Archaebacteria. J. Bacteriol. 170, 4315-4321.
64. Oberto, J. (2013). SyntTax: a web server linking synteny to prokaryotic taxonomy. BMC Bioinformatics 14:4. doi: 10.1186/1471-2105-14-4.
65. Odom, J. M., and Peck, H. D. (1981). Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria, Desulfovibrio sp. FEMS Microbiol. Lett. 12, 47-50. doi: 10.1111/j.1574-6968.1981.tb07609.x.
66. Oliveira, T. F., Franklin, E., Afonso, J. P., Khan, A. R., Oldham, N. J., Pereira, I. A. C., et al. (2011). Structural insights into dissimilatory sulfite reductases: structure of desulforubidin from Desulfomicrobium norvegicum. Front. Microbiol. 2:71. doi: 10.3389/fmicb.2011.00071.
67. Oliveira, T. F., Vonrhein, C., Matias, P. M., Venceslau, S. S., Pereira, I. A. C., and Archer, M. (2008). The crystal structure of Desulfovibrio vulgaris dissimilatory sulfite reductase bound to DsrC provides novel insights into the mechanism of sulfate respiration. J. Biol. Chem. 283, 34141-34149. doi: 10.1074/jbc.M805643200.
68. Pagala, V. R., Park, J., Reed, D. W., and Hartzell, P. L. (2002). Cellular localization of D-lactate dehydrogenase and NADH oxidase from Archaeoglobus fulgidus. Archaea 1, 95-104. doi: 10.1155/2002/297264.
69. Parey, K., Warkentin, E., Kroneck, P. M. H., and Ermler, U. (2010). Reaction cycle of the dissimilatory sulfite reductase from Archaeoglobus fulgidus. Biochemistry 49, 8912-8921. doi: 10.1021/bi100781f.
70. Parthasarathy, A., Kahnt, J., Chowdhury, N. P., and Buckel, W. (2013). Phenylalanine catabolism in Archaeoglobus fulgidus VC-16. Arch. Microbiol. 195, 781-797. doi: 10.1007/s00203-013-0925-3.
71. Peck, H. D. (1962). V. Comparative metabolism of inorganic sulfur compounds in microorganisms. Microbiol. Mol. Biol. Rev. 26, 67-94.
72. Pereira, I. A. C., Ramos, A. R., Grein, F., Marques, M. C., da Silva, S. M., and Venceslau, S. S. (2011). A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea. Front. Microbiol. 2:69. doi: 10.3389/fmicb.2011.00069.
73. Pereira, P. M., He, Q., Valente, F. M. A., Xavier, A. V., Zhou, J., Pereira, I. A. C., et al. (2008). Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis. Antonie Van Leeuwenhoek 93, 347-362. doi: 10.1007/s10482-007-9212-0.
74. Pinchuk, G. E., Rodionov, D. A., Yang, C., Li, X., Osterman, A. L., Dervyn, E., et al. (2009). Genomic reconstruction of Shewanella oneidensis MR-1 metabolism reveals a previously uncharacterized machinery for lactate utilization. Proc. Natl. Acad. Sci. U.S.A. 106, 2874-2879. doi: 10.1073/pnas.0806798106.
75. Pires, R. H., Lourenco, A. I., Morais, F., Teixeira, M., Xavier, A. V., Saraiva, L. M., et al. (2003). A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim. Biophys. Acta 1605, 67-82. doi: 10.1016/S0005-2728(03)00065-3.
76. Pires, R. H., Venceslau, S. S., Morais, F., Teixeira, M., Xavier, A. V., and Pereira, I. A. C. (2006). Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex-a membrane-bound redox complex involved in the sulfate respiratory pathway. Biochemistry 45, 249-262. doi: 10.1021/bi0515265.
77. Rabus, R., Hansen, T., and Widdel, F. (2006). "Dissimilatory sulfate-and sulfur-reducing prokaryotes," in The Prokaryotes Volume 2: Ecophysiology and Biochemistry, eds M. Dworkin, S. Falkow, E. Rosenberg, K. Schleifer, and E. Stackebrandt (New York, NY: Springer), 659-768.
78. Ramel, F., Amrani, A., Pieulle, L., Lamrabet, O., Voordouw, G., Seddiki, N., et al. (2013). Membrane-bound oxygen reductases of the anaerobic sulfate-reducing Desulfovibrio vulgaris Hildenborough: roles in oxygen defense and electron link with the periplasmic hydrogen oxidation. Microbiology 159, 2663-2673. doi: 10.1099/mic.0.071282-0.
79. Ramos, A. R., Keller, K. L., Wall, J. D., and Pereira, I. A. C. (2012). The Membrane QmoABC complex interacts directly with the dissimilatory adenosine 5'-phosphosulfate reductase in sulfate reducing bacteria. Front. Microbiol. 3:137. doi: 10.3389/fmicb.2012.00137.
80. Reed, D. W., and Hartzell, P. L. (1999). The Archaeoglobus fulgidus D-lactate dehydrogenase is a Zn2+ flavoprotein. J. Bacteriol. 181, 7580-7587.
81. Rodrigues, J. V., Abreu, I. A., Saraiva, L. M., and Teixeira, M. (2005). Rubredoxin acts as an electron donor for neelaredoxin in Archaeoglobus fulgidus. Biochem. Biophys. Res. Commun. 329, 1300-1305. doi: 10.1016/j.bbrc.2005.02.114.
82. Rohlin, L., Trent, J., and Salmon, K. (2005). Heat shock response of Archaeoglobus fulgidus. J. Bacteriol. 187, 6046-6057. doi: 10.1128/JB.187.17.6046-6057.2005.
83. Rubio, L. M., and Ludden, P. W. (2008). Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu. Rev. Microbiol. 62, 93-111. doi: 10.1146/annurev.micro.62.081307.162737.
84. Sato, T., Atomi, H., and Imanaka, T. (2007). Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315, 1003-1006. doi: 10.1126/science.1135999.
85. Schiffer, A., Parey, K., Warkentin, E., Diederichs, K., Huber, H., Stetter, K. O., et al. (2008). Structure of the dissimilatory sulfite reductase from the hyperthermophilic archaeon Archaeoglobus fulgidus. J. Mol. Biol. 379, 1063-1074. doi: 10.1016/j.jmb.2008.04.027.
86. Scholten, J. C., Culley, D. E., Brockman, F. J., Wu, G., and Zhang, W. (2007). Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer. Biochem. Biophys. Res. Commun. 352, 48-54. doi: 10.1016/j.bbrc.2006.10.164.
87. Shaw, A. J., Hogsett, D. A., and Lynd, L. R. (2009). Identification of the [FeFe] -hydrogenase responsible for hydrogen generation in Thermoanaerobacterium saccharolyticum and demonstration of increased ethanol yield via hydrogenase knockout. J. Bacteriol. 191, 6457-6464. doi: 10.1128/JB.00497-09.
88. So, C. M., and Young, L. Y. (1999). Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes. Appl. Environ. Microbiol. 65, 2969-2976.
89. Stahlmann, J., Warthmann, R., and Cypionka, H. (1991). Na+-dependent accumulation of sulfate and thiosulfate in marine sulfate-reducing bacteria. Arch. Microbiol. 155, 554-558. doi: 10.1007/BF00245349.
90. Steinsbu, B. O., Thorseth, I. H., Nakagawa, S., Inagaki, F., Lever, M. A., Engelen, B., et al. (2010). Archaeoglobus sulfaticallidus sp. nov., a novel thermophilic and facultatively lithoautotrophic sulfate-reducer isolated from black rust exposed to hot ridge flank crustal fluids. Int. J. Syst. Evol. Microbiol. 60, 2745-2752. doi: 10.1099/ijs.0.016105-0.
91. Stetter, K. O. (1988). Archaeoglobus fulgidus gen. nov., sp. nov.: a new taxon of extremely thermophilic Archaebacteria. Syst. Appl. Microbiol. 10, 172-173. doi: 10.1016/S0723-2020(88)80032-8.
92. Stetter, K. O., Lauerer, G., Thomm, M., and Neuner, A. (1987). Isolation of extremely thermophilic sulfate reducers: evidence for a novel branch of Archaebacteria. Science 236, 822-824. doi: 10.1126/science.236.4803.822.
93. Stoffels, L., Krehenbrink, M., Berks, B. C., and Unden, G. (2012). Thiosulfate reduction in Salmonella enterica is driven by the proton motive force. J. Bacteriol. 194, 475-485. doi: 10.1128/JB.06014-11.
94. Stokke, R., Hocking, W., Steinsbu, B. O., and Steen, I. H. (2013). Complete genome sequence of the thermophilic and facultatively chemolithoautotrophic sulfate reducer Archaeoglobus sulfaticallidus strain PM70-1T. Genome Announc. 1, 4-5. doi: 10.1128/genomeA.00406-13.
95. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550. doi: 10.1073/pnas.0506580102.
96. Takaki, Y., Shimamura, S., Nakagawa, S., Fukuhara, Y., Horikawa, H., Ankai, A., et al. (2010). Bacterial lifestyle in a deep-sea hydrothermal vent chimney revealed by the genome sequence of the thermophilic bacterium Deferribacter desulfuricans SSM1. DNA Res. 17, 123-137. doi: 10.1093/dnares/dsq005.
97. Taylor, B., and Zhulin, I. (1999). PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63, 479-506.
98. Thauer, R. K. (2012). The Wolfe cycle comes full circle. Proc. Natl. Acad. Sci. U.S.A. 109, 15084-15085. doi: 10.1073/pnas.1213193109.
99. 2 storage. Annu. Rev. Biochem. 79, 507-536. doi: 10.1146/annurev.biochem.030508.152103.
100. Thauer, R., Stackebrandt, E., and Hamilton, W. A. (2007). "Energy metabolism phylogenetic diversity of sulphate-reducing bacteria," in Sulphate-Reducing Bacteria, eds L. L. Barton and W. A. Hamilton (New York, NY: Cambridge University Press), 1-38.
101. Thomas, M. T., Shepherd, M., Poole, R. K., van Vliet, A. H. M., Kelly, D. J., and Pearson, B. M. (2011). Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on l-lactate. Environ. Microbiol. 13, 48-61. doi: 10.1111/j.1462-2920.2010.02307.x.
102. Tindall, B. J., Stetter, K. O., and Collins, M. D. (1989). A novel, fully saturated menaquinone from the thermophilic, sulphate-reducing Archaebacterium Archaeoglobus fulgidus. J. Gen. Microbiol. 135, 693-696. doi: 10.1099/00221287-135-3-693.
103. Tremblay, P., Zhang, T., Dar, S., Leang, C., and Lovley, D. (2013). The Rnf complex of Clostridium ljungdahlii is a proton-translocating ferredoxin: NAD+ oxidoreductase essential for autotrophic growth. MBio 4:e00406-12. doi: 10.1128/mBio.00406-12.
104. Vinogradov, A. D. (1998). Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) and the pseudo-reversible active/inactive enzyme transition. Biochim. Biophys. Acta 1364, 169-185. doi: 10.1016/S0005-2728(98)00026-7.
105. 2 fixation in Archaeoglobus lithotrophicus and the lack of carbon monoxide dehydrogenase in the heterotrophic A. profundus. Arch. Microbiol. 163, 112-118. doi: 10.1007/s002030050179.
106. Wall, J., Arkin, A., Balci, N., and Rapp-Giles, B. (2008). "Genetics and genomics of sulfate respiration in Desulfovibrio," in Microbial Sulfur Metabolism, eds C. Dahl and C. G. Friedrich (Berlin; Heidelberg: Springer), 1-12.
107. 2:NADP+ oxidoreductase with and without its substrates bound. EMBO J. 20, 6561-6569. doi: 10.1093/emboj/20.23.6561.
108. Watson, G. M. F., Yu, J., and Tabita, F. R. (1999). Unusual ribulose 1,5-bisphosphate carboxylase/oxygenase of anoxic archaea. J. Bacteriol. 181, 1569-1575.
109. Weinitschke, S., Denger, K., Cook, A. M., and Smits, T. H. M. (2007). The DUF81 protein TauE in Cupriavidus necator H16, a sulfite exporter in the metabolism of C2 sulfonates. Microbiology 153, 3055-3060. doi: 10.1099/mic.0.2007/009845-0.
110. Welte, C., and Deppenmeier, U. (2011). Membrane-bound electron transport in Methanosaeta thermophila. J. Bacteriol. 193, 2868-2870. doi: 10.1128/JB.00162-11.
111. Wolf, Y. I., Makarova, K. S., Yutin, N., and Koonin, E. V. (2012). Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol. Direct 7:46. doi: 10.1186/1745-6150-7-46.
112. Zane, G. M., Yen, H. B., and Wall, J. D. (2010). Effect of the deletion of qmoABC and the promoter-distal gene encoding a hypothetical protein on sulfate reduction in Desulfovibrio vulgaris Hildenborough. Appl. Environ. Microbiol. 76, 5500-5509. doi: 10.1128/AEM.00691-10.
113. Zarzycki, J., and Fuchs, G. (2011). Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus. Appl. Environ. Microbiol. 77, 6181-6188. doi: 10.1128/AEM.00705-11.
114. Zverlov, V., Klein, M., Lu, S., Friedrich, M. W., Kellermann, J., Stahl, D. A., et al. (2005). Lateral gene transfer of dissimilatory (bi)sulfite reductase revisited. J. Bacteriol. 187, 2203-2208. doi: 10.1128/JB.187.6.2203-2208.2005.