More Than 200 Genes Required for Methane Formation from H2 and CO2 and Energy Conservation Are Present in Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus
The hydrogenotrophic methanogens Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus can easily be mass cultured. They have therefore been used almost exclusively to study the biochemistry of methanogenesis from H2 and CO2, and the genomes of these two model organisms have been sequenced. The close relationship of the two organisms is reflected in their genomic architecture and coding potential. Within the 1,607 protein coding sequences (CDS) in common, we identified approximately 200 CDS required for the synthesis of the enzymes, coenzymes, and prosthetic groups involved in CO2 reduction to methane and in coupling this process with the phosphorylation of ADP. Approximately 20 additional genes, such as those for the biosynthesis of F430 and methanofuran and for the posttranslational modifications of the two methyl-coenzyme M reductases, remain to be identified. 1. Introduction In 1972, Zeikus and Wolfe [1] isolated Methanothermobacter thermautotrophicus (DSM 1053) (formerly Methanobacterium thermoautotrophicum strain ΔH) from sludge from the anaerobic sewage digestion plant in Urbana, Illinois, USA. This thermophile grew on H2 and CO2 as sole energy source (reaction 1) and CO2 as sole carbon source with doubling times of less than 5？h and to very high cell concentrations (1.5？g cells (dry mass) per L). For the first time, it became possible to obtain sufficient cell mass of a hydrogenotrophic methanogen for the purification of enzymes and coenzymes involved in CO2 reduction to methane. In 1978, Fuchs et al. [2] reported the isolation of Methanothermobacter marburgensis (DSM 2133) (formerly Methanobacterium thermoautotrophicum strain Marburg) from anaerobic sewage sludge in Marburg, Germany. The Marburg strain grew on H2 and CO2 even faster (doubling time less than 2？h) and to even higher cell concentrations (3？g cells (dry mass) per L) than the ΔH strain and was, therefore, subsequently used in Marburg and elsewhere for the study of methanogenesis. Most of what is presently known about the biochemistry of CO2 reduction to methane with H2 was worked out with either M. thermautotrophicus [3] or M. marburgensis [4–6] ( calculated for H2, CO2, and CH4 in the gas phase). The genome of M. thermautotrophicus (NC_000916) was one of the first genomes of Archaea to be sequenced [7] and that of M. marburgensis (NC_014408/CP001710) has just recently been announced [8]. This paper concentrates on the analysis of protein-coding sequences (CDS) required for the synthesis of enzymes, coenzymes, and prosthetic groups involved in CO2 reduction to
References
[1]
J. G. Zeikus and R. S. Wolfe, “Methanobacterium thermoautotrophicus Sp N, an anaerobic, autotrophic, extreme thermophile,” Journal of Bacteriology, vol. 109, no. 2, pp. 707–715, 1972.
[2]
G. Fuchs, E. Stupperich, and R. K. Thauer, “Acetate assimilation and the synthesis of alanine, aspartate and glutamate in Methanobacterium thermoautotrophicum,” Archives of Microbiology, vol. 117, no. 1, pp. 61–66, 1978.
[3]
A. A. DiMarco, T. A. Bobik, and R. S. Wolfe, “Unusual coenzymes of methanogenesis,” Annual Review of Biochemistry, vol. 59, pp. 355–394, 1990.
[4]
R. K. Thauer, “Biochemistry of methanogenesis: a tribute to Marjory Stephenson,” Microbiology, vol. 144, no. 9, pp. 2377–2406, 1998.
[5]
R. K. Thauer, A. K. Kaster, M. Goenrich, M. Schick, T. Hiromoto, and S. Shima, “Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage,” Annual Review of Biochemistry, vol. 79, pp. 507–536, 2010.
[6]
R. K. Thauer, A. K. Kaster, H. Seedorf, W. Buckel, and R. Hedderich, “Methanogenic archaea: ecologically relevant differences in energy conservation,” Nature Reviews Microbiology, vol. 6, no. 8, pp. 579–591, 2008.
[7]
D. R. Smith, L. A. Doucette-Stamm, C. Deloughery et al., “Complete genome sequence of Methanobacterium thermoautotrophicum ΔH: functional analysis and comparative genomics,” Journal of Bacteriology, vol. 179, no. 22, pp. 7135–7155, 1997.
[8]
H. Liesegang, A.-K. Kaster, A. Wiezer et al., “Complete genome sequence of Methanothermobacter marburgensis, a methanoarchaeon model organism,” Journal of Bacteriology, vol. 192, no. 21, pp. 5850–5851, 2010.
[9]
E. Bapteste, C. Brochier, and Y. Boucher, “Higher-level classification of the Archaea: evolution of methanogenesis and methanogens,” Archaea, vol. 1, no. 5, pp. 353–363, 2005.
[10]
S. Sakai, H. Imachi, S. Hanada, A. Ohashi, H. Harada, and Y. Kamagata, “Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage 'Rice Cluster I', and proposal of the new archaeal order Methanocellales ord. nov,” International Journal of Systematic and Evolutionary Microbiology, vol. 58, no. 4, pp. 929–936, 2008.
[11]
A. Jussofie and G. Gottschalk, “Further studies on the distribution of cytochromes in methanogenic bacteria,” FEMS Microbiology Letters, vol. 37, no. 1, pp. 15–18, 1986.
[12]
H. J. Abken, M. Tietze, J. Brodersen, S. B？umer, U. Beifuss, and U. Deppenmeier, “Isolation and characterization of methanophenazine and function of phenazines in membrane-bound electron transport of Methanosarcina mazei G？1,” Journal of Bacteriology, vol. 180, no. 8, pp. 2027–2032, 1998.
[13]
T. Stock, M. Selzer, and M. Rother, “In vivo requirement of selenophosphate for selenoprotein synthesis in archaea,” Molecular Microbiology, vol. 75, no. 1, pp. 149–160, 2010.
[14]
A. M. Guss, G. Kulkarni, and W. W. Metcalf, “Differences in hydrogenase Gene expression between Methanosarcina acetivorans and Methanosarcina barkeri,” Journal of Bacteriology, vol. 191, no. 8, pp. 2826–2833, 2009.
[15]
R. Conrad, “The global methane cycle: recent advances in understanding the microbial processes involved,” Environmental Microbiology Reports, vol. 1, no. 5, pp. 285–292, 2009.
[16]
R. Conrad, C. Erkel, and W. Liesack, “Rice Cluster I methanogens, an important group of Archaea producing greenhouse gas in soil,” Current Opinion in Biotechnology, vol. 17, no. 3, pp. 262–267, 2006.
[17]
A. Wasserfallen, J. N？lling, P. Pfister, J. Reeve, and E. C. De Macario, “Phylogenetic analysis of 18 thermophilic Methanobacterium isolates supports the proposals to create a new genus, Methanothermobacter gen. nov., and to reclassify several isolates in three species, Methanothermobacter thermautotrophicus comb. nov., Methanothermobacter wolfeii comb. nov., and Methanothermobacter marburgensis sp. nov,” International Journal of Systematic and Evolutionary Microbiology, vol. 50, no. 1, pp. 43–53, 2000.
[18]
F. U. Battistuzzi, A. Feijao, and S. B. Hedges, “A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land,” BMC Evolutionary Biology, vol. 4, article 44, 2004.
[19]
A. Brandis, R. K. Thauer, and K. O. Stetter, “Relatedness of strains ΔH and Marburg of Methanobacterium thermoautotrophicum,” Zentralblatt für Bakteriologie, Mikrobiologie und Hygiene, Abt. 1, Originale C, vol. 2, no. 4, pp. 311–317, 1981.
[20]
M. Bokranz, A. Klein, and L. Meile, “Complete nucleotide sequenc of plasmid pME2001 of Methanobacterium thermoautotrophicum (Marburg),” Nucleic Acids Research, vol. 18, no. 2, p. 363, 1990.
[21]
Y. Luo, T. Leisinger, and A. Wasserfallen, “Comparative sequence analysis of plasmids pME2001 and pME2200 of Methanothermobacter marburgensis strains Marburg and ZH3,” Plasmid, vol. 45, no. 1, pp. 18–30, 2001.
[22]
M. Jordan, L. Meile, and T. Leisinger, “Organization of Methanobacterium thermoautotrophicum bacteriophage ψM1 DNA,” Molecular and General Genetics, vol. 220, no. 1, pp. 161–164, 1989.
[23]
L. Meile, U. Jenal, D. Studer, M. Jordan, and T. Leisinger, “Characterization of ψM1, a virulent phage of Methanobacterium thermoautotrophicum Marburg,” Archives of Microbiology, vol. 152, no. 2, pp. 105–110, 1989.
[24]
J. Nolling, A. Groffen, and W. M. De Vos, “ΦF1 and ΦF3, two novel virulent, archaeal phages infecting different thermophilic strains of the genus Methanobacterium,” Journal of General Microbiology, vol. 139, no. 10, pp. 2511–2516, 1993.
[25]
Y. Luo, P. Pfister, T. Leisinger, and A. Wasserfallen, “The genome of archaeal prophage ψM100 encodes the lytic enzyme responsible for autolysis of Methanothermobacter wolfeii,” Journal of Bacteriology, vol. 183, no. 19, pp. 5788–5792, 2001.
[26]
P. A. Bertram, R. A. Schmitz, D. Linder, and R. K. Thauer, “Tungstate can substitute for molybdate in sustaining growth of Methanobacterium thermoautotrophicum. Identification and characterization of a tungsten isoenzyme of formylmethanofuran dehydrogenase,” Archives of Microbiology, vol. 161, no. 3, pp. 220–228, 1994.
[27]
P. Schoenheit, J. Moll, and R. K. Thauer, “Growth parameters ( , , ) of Methanobacterium thermoautotrophicum,” Archives of Microbiology, vol. 127, no. 1, pp. 59–65, 1980.
[28]
R. S. Tanner, M. J. McInerney, and D. P. Nagle, “Formate auxotroph of Methanobacterium thermoautotrophicum Marburg,” Journal of Bacteriology, vol. 171, no. 12, pp. 6534–6538, 1989.
[29]
G. Oberlies, G. Fuchs, and R. K. Thauer, “Acetate thiokinase and the assimilation of acetate in Methanobacterium thermoautotrophicum,” Archives of Microbiology, vol. 128, no. 2, pp. 248–252, 1980.
[30]
B. Eikmanns, R. Jaenchen, and R. K. Thauer, “Propionate assimilation by methanogenic bacteria,” Archives of Microbiology, vol. 136, no. 2, pp. 106–110, 1983.
[31]
R. Hüster and R. K. Thauer, “Pyruvate assimilation by Methanobacterium thermoautotrophicum,” FEMS Microbiology Letters, vol. 19, no. 2-3, pp. 207–209, 1983.
[32]
A. Tersteegen, D. Linder, R. K. Thauer, and R. Hedderich, “Structures and functions of four anabolic 2-oxoacid oxidoreductases in Methanobacterium thermoautotrophicum,” European Journal of Biochemistry, vol. 244, no. 3, pp. 862–868, 1997.
[33]
G. Diekert, H. H. Gilles, R. Jaenchen, and R. K. Thauer, “Incorporation of 8 succinate per mol nickel into factors F430 by Methanobacterium thermoautotrophicum,” Archives of Microbiology, vol. 128, no. 2, pp. 256–262, 1980.
[34]
G. Diekert, R. Jaenchen, and R. K. Thauer, “Biosynthetic evidence for a nickel tetrapyrrole structure of factor F430 from Methanobacterium thermoautotrophicum,” FEBS Letters, vol. 119, no. 1, pp. 118–120, 1980.
[35]
R. Jaenchen, G. Diekert, and R. K. Thauer, “Incorporation of methionine-derived methyl groups into factor F430 by Methanobacterium thermoautotrophicum,” FEBS Letters, vol. 130, no. 1, pp. 133–136, 1981.
[36]
R. Jaenchen, P. Schonheit, and R. K. Thauer, “Studies on the biosynthesis of coenzyme F420 in methanogenic bacteria,” Archives of Microbiology, vol. 137, no. 4, pp. 362–365, 1984.
[37]
B. Mukhopadhyay, S. F. Stoddard, and R. S. Wolfe, “Purification, regulation, and molecular and biochemical characterization of pyruvate carboxylase from Methanobacterium thermoautotrophicum strain ΔH,” Journal of Biological Chemistry, vol. 273, no. 9, pp. 5155–5166, 1998.
[38]
J. Nolling, D. Hahn, W. Ludwig, and W. M. De Vos, “Phylogenetic analysis of thermophilic Methanobacterium Sp—evidence for a formate-utilizing ancestor,” Systematic and Applied Microbiology, vol. 16, no. 2, pp. 208–215, 1993.
[39]
D. H. Haft and W. T. Self, “Orphan SelD proteins and selenium-dependent molybdenum hydroxylases,” Biology Direct, vol. 3, article 4, 2008.
[40]
Y. Itoh, S. I. Sekine, E. Matsumoto et al., “Structure of selenophosphate synthetase essential for selenium incorporation into proteins and RNAs,” Journal of Molecular Biology, vol. 385, no. 5, pp. 1456–1469, 2009.
[41]
S. C. Leahy, W. J. Kelly, E. Altermann et al., “The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions,” PloS ONE, vol. 5, no. 1, Article ID e8926, 2010.
[42]
X. Ding, W. J. Yang, H. Min, X. T. Peng, H. Y. Zhou, and Z. M. Lu, “Isolation and characterization of a new strain of Methanothermobacter marburgensis DX01 from hot springs in China,” Anaerobe, vol. 16, no. 1, pp. 54–59, 2010.
[43]
S. B. Needleman and C. D. Wunsch, “A general method applicable to the search for similarities in the amino acid sequence of two proteins,” Journal of Molecular Biology, vol. 48, no. 3, pp. 443–453, 1970.
[44]
S. Cheng, D. Xing, D. F. Call, and B. E. Logan, “Direct biological conversion of electrical current into methane by electromethanogenesis,” Environmental Science and Technology, vol. 43, no. 10, pp. 3953–3958, 2009.
[45]
M. Villano, F. Aulenta, C. Ciucci, T. Ferri, A. Giuliano, and M. Majone, “Bioelectrochemical reduction of CO2 to CH4 via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture,” Bioresource Technology, vol. 101, no. 9, pp. 3085–3090, 2010.
[46]
K. H. Nealson, “Geomicrobiology: sediment reactions defy dogma,” Nature, vol. 463, no. 7284, pp. 1033–1034, 2010.
[47]
L. P. Nielsen, N. Risgaard-Petersen, H. Fossing, P. B. Christensen, and M. Sayama, “Electric currents couple spatially separated biogeochemical processes in marine sediment,” Nature, vol. 463, no. 7284, pp. 1071–1074, 2010.
[48]
G. Reguera, K. D. McCarthy, T. Mehta, J. S. Nicoll, M. T. Tuominen, and D. R. Lovley, “Extracellular electron transfer via microbial nanowires,” Nature, vol. 435, no. 7045, pp. 1098–1101, 2005.
[49]
C. Thoma, M. Frank, R. Rachel et al., “The Mth60 fimbriae of Methanothermobacter thermoautotrophicus are functional adhesins,” Environmental Microbiology, vol. 10, no. 10, pp. 2785–2795, 2008.
[50]
M. W. Friedrich, “Methyl-coenzyme M reductase genes: unique functional markers for methanogenic and anaerobic methane-oxidizing Archaea,” Methods in Enzymology, vol. 397, pp. 428–442, 2005.
[51]
S. Kurtz, A. Phillippy, A. L. Delcher et al., “Versatile and open software for comparing large genomes,” Genome Biology, vol. 5, no. 2, p. 12, 2004.
[52]
P. Vermeij, R. J. T. Van Der Steen, J. T. Keltjens, G. D. Vogels, and T. Leisinger, “Coenzyme F390 synthetase from Methanobacterium thermoautotrophicum Marburg belongs to the superfamily of adenylate-forming enzymes,” Journal of Bacteriology, vol. 178, no. 2, pp. 505–510, 1996.
[53]
J. Filée, P. Siguier, and M. Chandler, “Insertion sequence diversity in Archaea,” Microbiology and Molecular Biology Reviews, vol. 71, no. 1, pp. 121–157, 2007.
[54]
H. Deveau, J. E. Garneau, and S. Moineau, “CRISPR/Cas system and its role in phage-bacteria interactions,” Annual Review of Microbiology, vol. 64, pp. 475–493, 2010.
[55]
F. V. Karginov and G. J. Hannon, “The CRISPR system: small RNA-guided defense in bacteria and archaea,” Molecular Cell, vol. 37, no. 1, pp. 7–19, 2010.
[56]
L. A. Marraffini and E. J. Sontheimer, “Self versus non-self discrimination during CRISPR RNA-directed immunity,” Nature, vol. 463, no. 7280, pp. 568–571, 2010.
[57]
R. K. Lillest？l, P. Redder, R. A. Garrett, and K. Brügger, “A putative viral defence mechanism in archaeal cells,” Archaea, vol. 2, no. 1, pp. 59–72, 2006.
[58]
I. A. Berg, D. Kockelkorn, W. H. Ramos-Vera et al., “Autotrophic carbon fixation in archaea,” Nature Reviews Microbiology, vol. 8, no. 6, pp. 447–460, 2010.
[59]
L. M. I. de Poorter, W. J. Geerts, and J. T. Keltjens, “Hydrogen concentrations in methane-forming cells probed by the ratios of reduced and oxidized coenzyme F420,” Microbiology, vol. 151, no. 5, pp. 1697–1705, 2005.
[60]
A. K. Kaster, J. Moll, K. Parey, and R. Thauer, “Coupling of ferredoxin- and heterodisulfide reduction with H2 via electron bifurcation in hydrogenotrophic methanogenic archaea,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 7, pp. 2981–2986, 2011.
[61]
P. A. Bertram and R. K. Thauer, “Thermodynamics of the formylmethanofuran dehydrogenase reaction in Methanobacterium thermoautotrophicum,” European Journal of Biochemistry, vol. 226, no. 3, pp. 811–818, 1994.
[62]
K. C. Costa, P. M. Wong, T. Wang et al., “Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 24, pp. 11050–11055, 2010.
[63]
J. Nolling, T. D. Pihl, A. Vriesema, and J. N. Reeve, “Organization and growth phase-dependent transcription of methane genes in two regions of the Methanobacterium thermoautotrophicum genome,” Journal of Bacteriology, vol. 177, no. 9, pp. 2460–2468, 1995.
[64]
T. D. Pihl, S. Sharma, and J. N. Reeve, “Growth phase-dependent transcription of the genes that encode the two methyl coenzyme M reductase isoenzymes and -methyltetrahydromethanopterin:Coenzyme M methyltransferase in Methanobacterium thermoautotrophicum ΔH,” Journal of Bacteriology, vol. 176, no. 20, pp. 6384–6391, 1994.
[65]
N. Hamann, G. J. Mander, J. E. Shokes, R. A. Scott, M. Bennati, and R. Hedderich, “A cysteine-rich CCG domain contains a novel [4Fe-4S] cluster binding motif as deduced from studies with subunit B of heterodisulfide reductase from Methanothermobacter marburgensis,” Biochemistry, vol. 46, no. 44, pp. 12875–12885, 2007.
[66]
R. Hedderich, J. Koch, D. Linder, and R. K. Thauer, “The heterodisulfide reductase from Methanobacterium thermoautotrophicum contains sequence motifs characteristic of pyridine-nucleotide-dependent thioredoxin reductases,” European Journal of Biochemistry, vol. 225, no. 1, pp. 253–261, 1994.
[67]
I. Anderson, L. E. Ulrich, B. Lupa et al., “Genomic characterization of methanomicrobiales reveals three classes of methanogens,” PLoS ONE, vol. 4, no. 6, Article ID e5797, 2009.
[68]
A. B？ck, P. W. King, M. Blokesch, and M. C. Posewitz, “Maturation of Hydrogenases,” Advances in Microbial Physiology, vol. 51, pp. 1–71, 2006.
[69]
C. Afting, A. Hochheimer, and R. K. Thauer, “Function of H-forming methylenetetrahydromethanopterin dehydrogenase from Methanobacterium thermoautotrophicum in coenzyme F420 reduction with H2,” Archives of Microbiology, vol. 169, no. 3, pp. 206–210, 1998.
[70]
E. L. Hendrickson and J. A. Leigh, “Roles of coenzyme F420-reducing hydrogenases and hydrogen- and F420-dependent methylenetetrahydromethanopterin dehydrogenases in reduction of F420 and production of hydrogen during methanogenesis,” Journal of Bacteriology, vol. 190, no. 14, pp. 4818–4821, 2008.
[71]
B. Lupa, E. L. Hendrickson, J. A. Leigh, and W. B. Whitman, “Formate-dependent H2production by the mesophilic methanogen Methanococcus maripaludis,” Applied and Environmental Microbiology, vol. 74, no. 21, pp. 6584–6590, 2008.
[72]
C. Welte, V. Kallnik, M. Grapp, G. Bender, S. Ragsdale, and U. Deppenmeier, “Function of Ech hydrogenase in ferredoxin-dependent, membrane-bound electron transport in Methanosarcina mazei,” Journal of Bacteriology, vol. 192, no. 3, pp. 674–678, 2010.
[73]
T. A. Major, Y. Liu, and W. B. Whitman, “Characterization of energy-conserving hydrogenase B in Methanococcus maripaludis,” Journal of Bacteriology, vol. 192, no. 15, pp. 4022–4030, 2010.
[74]
I. Porat, W. Kim, E. L. Hendrickson et al., “Disruption of the operon encoding Ehb hydrogenase limits anabolic CO2 assimilation in the archaeon Methanococcus maripaludis,” Journal of Bacteriology, vol. 188, no. 4, pp. 1373–1380, 2006.
[75]
A. Tersteegen and R. Hedderich, “Methanobacterium thermoautotrophicum encodes two multisubunit membrane- bound [NiFe] hydrogenases. Transcription of the operons and sequence analysis of the deduced proteins,” European Journal of Biochemistry, vol. 264, no. 3, pp. 930–943, 1999.
[76]
R. Hedderich and L. Forzi, “Energy-converting [NiFe] hydrogenases: more than just H2activation,” Journal of Molecular Microbiology and Biotechnology, vol. 10, no. 2-4, pp. 92–104, 2006.
[77]
J. A. Vorholt and R. K. Thauer, “Molybdenum and tungsten enzymes in C1 metabolism,” Metal Ions in Biological Systems, vol. 39, pp. 571–619, 2002.
[78]
A. Hochheimer, R. Hedderich, and R. K. Thauer, “The formylmethanofuran dehydrogenase isoenzymes in Methanobacterium wolfei and Methanobacterium thermoautotrophicum: induction of the molybdenum isoenzyme by molybdate and constitutive synthesis of the tungsten isoenzyme,” Archives of Microbiology, vol. 170, no. 5, pp. 389–393, 1998.
[79]
A. Hochheimer, D. Linder, R. K. Thauer, and R. Hedderich, “The molybdenum formylmethanofuran dehydrogenase operon and the tungsten formylmethanofuran dehydrogenase operon from Methanobacterium thermoautotrophicum. Structures and transcriptional regulation,” European Journal of Biochemistry, vol. 242, no. 1, pp. 156–162, 1996.
[80]
W. Grabarse, M. Vaupel, J. A. Vorholt et al., “The crystal structure of methenyltetrahydromethanopterin cyclohydrolase from the hyperthermophilic archaeon Methanopyrus kandleri,” Structure, vol. 7, no. 10, pp. 1257–1268, 1999.
[81]
S. Shima, E. Warkentin, R. K. Thauer, and U. Ermler, “Structure and function of enzymes involved in the methanogenic pathway utilizing carbon dioxide and molecular hydrogen,” Journal of Bioscience and Bioengineering, vol. 93, no. 6, pp. 519–530, 2002.
[82]
B. Buchenau and R. K. Thauer, “Tetrahydrofolate-specific enzymes in Methanosarcina barkeri and growth dependence of this methanogenic archaeon on folic acid or p-aminobenzoic acid,” Archives of Microbiology, vol. 182, no. 4, pp. 313–325, 2004.
[83]
G. Gottschalk and R. K. Thauer, “The Na+-translocating methyltransferase complex from methanogenic archaea,” Biochimica et Biophysica Acta, vol. 1505, no. 1, pp. 28–36, 2001.
[84]
D. H. Shin, “Preliminary structural studies on the MtxX protein from Methanococcus jannaschii,” Acta Crystallographica Section D: Biological Crystallography, vol. 64, no. 4, pp. 300–303, 2008.
[85]
D. Stroup and J. N. Reeve, “Identification of the mcrC gene product in Methanococcus vannielii,” FEMS Microbiology Letters, vol. 111, no. 1, pp. 129–134, 1993.
[86]
C. H. Kuhner, B. D. Lindenbach, and R. S. Wolfe, “Component A2 of methylcoenzyme M reductase system from Methanobacterium thermoautotrophicum ΔH: nucleotide sequence and functional expression by Escherichia coli,” Journal of Bacteriology, vol. 175, no. 10, pp. 3195–3203, 1993.
[87]
R. Hedderich, S. P. J. Albracht, D. Linder, J. Koch, and R. K. Thauer, “Isolation and characterization of polyferredoxin from Methanobacterium thermoautotrophicum. The mvhB gene product of the methylviologen-reducing hydrogenase operon,” FEBS Letters, vol. 298, no. 1, pp. 65–68, 1992.
[88]
T. Lienard, B. Becher, M. Marschall, S. Bowien, and G. Gottschalk, “Sodium ion translocation by N-methyltetrahydromethanopterin:coenzyme M methyltransferase from Methanosarcina mazei G？1 reconstituted in ether lipid liposomes,” European Journal of Biochemistry, vol. 239, no. 3, pp. 857–864, 1996.
[89]
K. Y. Pisa, H. Huber, M. Thomm, and V. Müller, “A sodium ion-dependent AA ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus,” FEBS Journal, vol. 274, no. 15, pp. 3928–3938, 2007.
[90]
M. Vidová and P. ？migáň, “Unique structural and functional properties of AA ATPase/synthase from archaeaUnikátne ？truktúrne a funk？né vlastnosti AA ATPáz/syntáz Z archaea,” Chemicke Listy, vol. 104, no. 5, pp. 309–317, 2010.
[91]
S. ？urín, L. ？uboňová, A. I. Majerník, P. McDermott, J. P. J. Chong, and P. ？migáň, “Isolation and characterization of an amiloride-resistant mutant of Methanothermobacter thermautotrophicus possessing a defective Na+/H+ antiport,” FEMS Microbiology Letters, vol. 269, no. 2, pp. 301–308, 2007.
[92]
S. E. McGlynn, E. S. Boyd, E. M. Shepard et al., “Identification and characterization of a novel member of the radical AdoMet enzyme superfamily and implications for the biosynthesis of the Hmd hydrogenase active site cofactor,” Journal of Bacteriology, vol. 192, no. 2, pp. 595–598, 2010.
[93]
S. Shima and R. K. Thauer, “A third type of hydrogenase catalyzing H2activation,” Chemical Record, vol. 7, no. 1, pp. 37–46, 2007.
[94]
P. Schoenheit, J. Moll, and R. K. Thauer, “Nickel, cobalt, and molybdenum requirement for growth of Methanobacterium thermoautotrophicum,” Archives of Microbiology, vol. 123, no. 1, pp. 105–107, 1979.
[95]
D. Vinella, C. Brochier-Armanet, L. Loiseau, E. Talla, and F. Barras, “Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers,” PLoS Genetics, vol. 5, no. 5, Article ID e1000497, 2009.
[96]
J. M. Boyd, R. M. Drevland, D. M. Downs, and D. E. Graham, “Archaeal ApbC/Nbp35 homologs function as iron-sulfur cluster carrier proteins,” Journal of Bacteriology, vol. 191, no. 5, pp. 1490–1497, 2009.
[97]
J. M. Boyd, J. L. Sondelski, and D. M. Downs, “Bacterial apbC protein has two biochemical activities that are required for in vivo function,” Journal of Biological Chemistry, vol. 284, no. 1, pp. 110–118, 2009.
[98]
Y. Liu, M. Sieprawska-Lupa, W. B. Whitman, and R. H. White, “Cysteine is not the sulfur source for iron-sulfur cluster and methionine biosynthesis in the methanogenic archaeon Methanococcus maripaludis,” Journal of Biological Chemistry, vol. 285, no. 42, pp. 31923–31929, 2010.
[99]
G. Schwarz, R. R. Mendel, and M. W. Ribbe, “Molybdenum cofactors, enzymes and pathways,” Nature, vol. 460, no. 7257, pp. 839–847, 2009.
[100]
B. Krautler, J. Moll, and R. K. Thauer, “The corrinoid from Methanobacterium thermoautotrophicum (Marburg strain). Spectroscopic structure analysis and identifcation as Co(β)-cyano-5'-hydroxybenzimidazolyl-cobamide (factor III),” European Journal of Biochemistry, vol. 162, no. 2, pp. 275–278, 1987.
[101]
S. Frank, E. Deery, A. A. Brindley et al., “Elucidation of substrate specificity in the cobalamin (vitamin B12 ) biosynthetic methyltransferases: structure and function of the C20 methyltransferase (CbiL) from Methanothermobacter thermautotrophicus,” Journal of Biological Chemistry, vol. 282, no. 33, pp. 23957–23969, 2007.
[102]
D. A. Rodionov, A. G. Vitreschak, A. A. Mironov, and M. S. Gelfand, “Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes,” Journal of Biological Chemistry, vol. 278, no. 42, pp. 41148–41159, 2003.
[103]
K. Sauer and R. K. Thauer, “The role of corrinoids in methanogenesis,” in Chemistry and Biochemistry of B12, R. Banerjee, Ed., John Wiley & Sons, New York, NY, USA, 1999.
[104]
J. D. Woodson and J. C. Escalante-Semerena, “CbiZ, an amidohydrolase enzyme required for salvaging the coenzyme B precursor cobinamide in archaea,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 10, pp. 3591–3596, 2004.
[105]
J. D. Woodson and J. C. Escalante-Semerena, “The cbiS gene of the archaeon Methanopyrus kandleri AV19 encodes a bifunctional enzyme with adenosylcobinamide amidohydrolase and α-ribazole-phosphate phosphatase activities,” Journal of Bacteriology, vol. 188, no. 12, pp. 4227–4235, 2006.
[106]
J. D. Woodson, C. L. Zayas, and J. C. Escalante-Semerena, “A new pathway for salvaging the coenzyme B12 precursor cobinamide in archaea requires cobinamide-phosphate synthase (CbiB) enzyme activity,” Journal of Bacteriology, vol. 185, no. 24, pp. 7193–7201, 2003.
[107]
E. F. Johnson and B. Mukhopadhyay, “A new type of sulfite reductase, a novel coenzyme F420-dependent enzyme, from the methanarchaeon Methanocaldococcus jannaschii,” Journal of Biological Chemistry, vol. 280, no. 46, pp. 38776–38786, 2005.
[108]
A. Pfaltz, A. Kobelt, R. Hunster, and R. K. Thauer, “Biosynthesis of coenzyme F430 in methanogenic bacteria. Identification of 15,173-seco-F430-173-acid as an intermediate,” European Journal of Biochemistry, vol. 170, no. 1-2, pp. 459–467, 1988.
[109]
J. Lundqvist, D. Elmlund, D. Heldt et al., “The AAA(+) motor complex of subunits CobS and CobT of cobaltochelatase visualized by single particle electron microscopy,” Journal of Structural Biology, vol. 167, no. 3, pp. 227–234, 2009.
[110]
C. R. Staples, S. Lahiri, J. Raymond, L. Von Herbulis, B. Mukhophadhyay, and R. E. Blankenship, “Expression and association of group IV nitrogenase NifD and NifH homologs in the non-nitrogen-fixing archaeon Methanocaldococcus jannaschii,” Journal of Bacteriology, vol. 189, no. 20, pp. 7392–7398, 2007.
[111]
N. Muraki, J. Nomata, K. Ebata et al., “X-ray crystal structure of the light-independent protochlorophyllide reductase,” Nature, vol. 465, no. 7294, pp. 110–114, 2010.
[112]
A. Meyerdierks, M. Kube, I. Kostadinov et al., “Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group,” Environmental Microbiology, vol. 12, no. 2, pp. 422–439, 2010.
[113]
S. Mayr, C. Latkoczy, M. Krüger et al., “Structure of an F430 variant from archaea associated with anaerobic oxidation of methane,” Journal of the American Chemical Society, vol. 130, no. 32, pp. 10758–10767, 2008.
[114]
R. K. Thauer and S. Shima, “Methane as fuel for anaerobic microorganisms,” Annals of the New York Academy of Sciences, vol. 1125, pp. 158–170, 2008.
[115]
M. Vandevenne, P. Filee, N. Scarafone et al., “The Bacillus licheniformis BlaP β-lactamase as a model protein scaffold to study the insertion of protein fragments,” Protein Science, vol. 16, no. 10, pp. 2260–2271, 2007.
[116]
D. E. Graham and R. H. White, “Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics,” Natural Product Reports, vol. 19, no. 2, pp. 133–147, 2002.
[117]
F. Forouhar, M. Abashidze, H. Xu et al., “Molecular insights into the biosynthesis of the F420 coenzyme,” Journal of Biological Chemistry, vol. 283, no. 17, pp. 11832–11840, 2008.
[118]
L. L. Grochowski, H. Xu, and R. H. White, “Identification and characterization of the 2-phospho-L-lactate guanylyltransferase involved in coenzyme F420 biosynthesis,” Biochemistry, vol. 47, no. 9, pp. 3033–3037, 2008.
[119]
L. L. Grochowski, H. Xu, and R. H. White, “Identification of lactaldehyde dehydrogenase in Methanocaldococcus jannaschii and its involvement in production of lactate for F420 biosynthesis,” Journal of Bacteriology, vol. 188, no. 8, pp. 2836–2844, 2006.
[120]
B. Nocek, E. Evdokimova, M. Proudfoot et al., “Structure of an amide bond forming F420:gamma-glutamyl ligase from Archaeoglobus fulgidus—a member of a new family of non-ribosomal peptide synthases,” Journal of Molecular Biology, vol. 372, no. 2, pp. 456–469, 2007.
[121]
H. Li, H. Xu, D. E. Graham, and R. H. White, “Glutathione synthetase homologs encode α-L-glutamate ligases for methanogenic coenzyme F420 and tetrahydrosarcinapterin biosyntheses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 17, pp. 9785–9790, 2003.
[122]
H. Seedorf, A. Dreisbach, R. Hedderich, S. Shima, and R. K. Thauer, “F420H2 oxidase (FprA) from Methanobrevibacter arboriphilus, a coenzyme F420-dependent enzyme involved in O2 detoxification,” Archives of Microbiology, vol. 182, no. 2-3, pp. 126–137, 2004.
[123]
K. Ceh, U. Demmer, E. Warkentin et al., “Structural basis of the hydride transfer mechanism in F420-dependent methylenetetrahydromethanopterin dehydrogenase,” Biochemistry, vol. 48, no. 42, pp. 10098–10105, 2009.
[124]
H. Seedorf, C. H. Hagemeier, S. Shima, R. K. Thauer, E. Warkentin, and U. Ermler, “Structure of coenzyme F420H2 oxidase (FprA), a di-iron flavoprotein from methanogenic Archaea catalyzing the reduction of O2 to H2O,” FEBS Journal, vol. 274, no. 6, pp. 1588–1599, 2007.
[125]
E. F. Johnson and B. Mukhopadhyay, “A novel coenzyme F420 dependent sulfite reductase and a small sulfite reductase in methanogenic archaea,” in Microbial Sulfur Metabolism, C. D. A. C. G. Friedrich, Ed., pp. 202–216, Springer, Berlin, Germany, 2008.
[126]
P. C. Raemakers-Franken, R. J.M. Brand, A. J. Kortstee, C. Van der Drift, and G. D. Vogels, “Ammonia assimilation and glutamate incorporation in coenzyme F420 derivatives of Methanosarcina barkeri,” Antonie van Leeuwenhoek, International Journal of General, vol. 59, no. 4, pp. 243–248, 1991.
[127]
W. B. White and J. G. Ferry, “Identification of formate dehydrogenase-specific mRNA species and nucleotide sequence of the fdhC gene of Methanobacterium formicicum,” Journal of Bacteriology, vol. 174, no. 15, pp. 4997–5004, 1992.
[128]
K. Ownby, H. Xu, and R. H. White, “A Methanocaldococcus jannaschii archaeal signature gene encodes for a 5-formaminoimidazole-4-carboxamide-1-β-D-ribofuranosyl 5′- monophosphate synthetase: a new enzyme in purine biosynthesis,” Journal of Biological Chemistry, vol. 280, no. 12, pp. 10881–10887, 2005.
[129]
A. B. Waight, J. Love, and DA. N. Wang, “Structure and mechanism of a pentameric formate channel,” Nature Structural & Molecular Biology, vol. 17, no. 1, pp. 31–37, 2010.
[130]
G. E. Wood, A. K. Haydock, and J. A. Leigh, “Function and regulation of the formate dehydrogenase genes of the methanogenic archaeon Methanococcus maripaludis,” Journal of Bacteriology, vol. 185, no. 8, pp. 2548–2554, 2003.
[131]
N. D. Kezmarsky, H. Xu, D. E. Graham, and R. H. White, “Identification and characterization of a L-tyrosine decarboxylase in Methanocaldococcus jannaschii,” Biochimica et Biophysica Acta, vol. 1722, no. 2, pp. 175–182, 2005.
[132]
Z. Mashhadi, H. Xu, and R. H. White, “An Fe2+-dependent cyclic phosphodiesterase catalyzes the hydrolysis of 7,8-dihydro-D-neopterin , -cyclic phosphate in methanopterin biosynthesis,” Biochemistry, vol. 48, no. 40, pp. 9384–9392, 2009.
[133]
M. E. Bechard, D. Garcia, D. Greene, and M. E. Rasche, “Overproduction, characterization, and site-directed mutagenisis of RFAP synthase from the methanogen Methanothermobacter thermoautotrophicus delta H,” in Proceedings of the eneral Meeting of the Americam Society for Microbiology, 2003.
[134]
F. Li, C. H. Hagemeier, H. Seedorf, G. Gottschalk, and R. K. Thauer, “Re-citrate synthase from Clostridium kluyveri is phylogenetically related to homocitrate synthase and isopropylmalate synthase rather than to Si-citrate synthase,” Journal of Bacteriology, vol. 189, no. 11, pp. 4299–4304, 2007.
[135]
R. M. Drevland, Y. Jia, D. R. J. Palmer, and D. E. Graham, “Methanogen homoaconitase catalyzes both hydrolyase reactions in coenzyme B biosynthesis,” Journal of Biological Chemistry, vol. 283, no. 43, pp. 28888–28896, 2008.
[136]
R. J. P. Williams and J. J. R. Frausto da Silva, The Natural Selection of the Chemical Elements, Oxford University Press, Oxford, UK, 1996.
[137]
Y. Zhang, D. A. Rodionov, M. S. Gelfand, and V. N. Gladyshev, “Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization,” BMC Genomics, vol. 10, article 78, 2009.
[138]
M. Kammler, C. Schon, and K. Hantke, “Characterization of the ferrous iron uptake system of Escherichia coli,” Journal of Bacteriology, vol. 175, no. 19, pp. 6212–6219, 1993.
[139]
S. C. Wang, A. V. Dias, and D. B. Zamble, “The “metallo-specific” response of proteins: a perspective based on the Escherichia coli transcriptional regulator NikR,” Dalton Transactions, no. 14, pp. 2459–2466, 2009.
[140]
S. Leitch, M. J. Bradley, J. L. Rowe, P. T. Chivers, and M. J. Maroney, “Nickel-specific response in the transcriptional regulator, Escherichia coli NikR,” Journal of the American Chemical Society, vol. 129, no. 16, pp. 5085–5095, 2007.
[141]
M. Hattori, N. Iwase, N. Furuya et al., “Mg2+-dependent gating of bacterial MgtE channel underlies Mg2+ homeostasis,” EMBO Journal, vol. 28, no. 22, pp. 3602–3612, 2009.
[142]
M. Van？ek, M. Vidová, A. I. Majerník, and P. ？migáň, “Methanogenesis is Ca2+dependent in Methanothermobacter thermautotrophicus strain ΔH,” FEMS Microbiology Letters, vol. 258, no. 2, pp. 269–273, 2006.
[143]
B. De Hertogh, A. C. Lantin, P. V. Baret, and A. Goffeau, “The archaeal P-type ATPases,” Journal of Bioenergetics and Biomembranes, vol. 36, no. 1, pp. 135–142, 2004.
[144]
P. Schonheit, D. B. Beimborn, and H. J. Perski, “Potassium accumulation in growing Methanobacterium thermoautotrophicum and its relation to the electrochemical proton gradient,” Archives of Microbiology, vol. 140, no. 2-3, pp. 247–251, 1984.
[145]
J. Glasemacher, A. Siebers, K. Altendorf, and P. Sch？nheit, “Low-affinity potassium uptake system in the archaeon Methanobacterium thermoautotrophicum: overproduction of a 31-kilodalton membrane protein during growth on low-potassium medium,” Journal of Bacteriology, vol. 178, no. 3, pp. 728–734, 1996.
[146]
W. T. Self, A. M. Grunden, A. Hasona, and K. T. Shanmugam, “Molybdate transport,” Research in Microbiology, vol. 152, no. 3-4, pp. 311–321, 2001.
[147]
Y. Zhang and V. N. Gladyshev, “Molybdoproteomes and evolution of molybdenum utilization,” Journal of Molecular Biology, vol. 379, no. 4, pp. 881–899, 2008.
[148]
L. E. Bevers, P. L. Hagedoorn, G. C. Krijger, and W. R. Hagen, “Tungsten transport protein A (WtpA) in Pyrococcus furiosus: the first member of a new class of tungstate and molybdate transporters,” Journal of Bacteriology, vol. 188, no. 18, pp. 6498–6505, 2006.
[149]
S. Gerber, M. Comellas-Bigler, B. A. Goetz, and K. P. Locher, “Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter,” Science, vol. 321, no. 5886, pp. 246–250, 2008.
[150]
M. Aguena and B. Spira, “Transcriptional processing of the pst operon of Escherichia coli,” Current Microbiology, vol. 58, no. 3, pp. 264–267, 2009.
[151]
C. Afting, E. Kremmer, C. Brucker, A. Hochheimer, and R. K. Thauer, “Regulation of the synthesis of H2-forming methylenetetrahydromethanopterin dehydrogenase (Hmd) and of HmdII and HmdIII in Methanothermobacter marburgensis,” Archives of Microbiology, vol. 174, no. 4, pp. 225–232, 2000.
[152]
D. Osman and J. S. Cavet, “Bacterial metal-sensing proteins exemplified by ArsR-SmtB family repressors,” Natural Product Reports, vol. 27, no. 5, pp. 668–680, 2010.
[153]
A. Hochheimer, R. Hedderich, and R. K. Thauer, “The DNA binding protein Tfx from Methanobacterium thermoautotrophicum: structure, DNA binding properties and transcriptional regulation,” Molecular Microbiology, vol. 31, no. 2, pp. 641–650, 1999.
[154]
L. G. Bonacker, S. Baudner, and R. K. Thauer, “Differential expression of the two methyl-coenzyme M reductases in Methanobacterium thermoautotrophicum as determined immunochemically via isoenzyme-speficic antisera,” European Journal of Biochemistry, vol. 206, no. 1, pp. 87–92, 1992.
[155]
R. M. Morgan, T. D. Pihl, J. N？lling, and J. N. Reeve, “Hydrogen regulation of growth, growth yields, and methane gene transcription in Methanobacterium thermoautotrophicumδH,” Journal of Bacteriology, vol. 179, no. 3, pp. 889–898, 1997.
[156]
N. Shinzato, M. Enoki, H. Sato, K. Nakamura, T. Matsui, and Y. Kamagata, “Specific DNA binding of a potential transcriptional regulator, inosine -monophosphate dehydrogenase-related protein VII, to the promoter region of a methyl coenzyme M reductase I-encoding operon retrieved from Methanothermobacter thermautotrophicus strain ΔH,” Applied and Environmental Microbiology, vol. 74, no. 20, pp. 6239–6247, 2008.
[157]
O. Lenz, M. Bernhard, T. Buhrke, E. Schwartz, and B. Friedrich, “The hydrogen-sensing apparatus in Ralstonia eutropha,” Journal of Molecular Microbiology and Biotechnology, vol. 4, no. 3, pp. 255–262, 2002.
[158]
J. A. Leigh and J. A. Dodsworth, “Nitrogen regulation in bacteria and archaea,” Annual Review of Microbiology, vol. 61, pp. 349–377, 2007.
[159]
T. J. Lie, E. L. Hendrickson, U. M. Niess, B. C. Moore, A. K. Haydock, and J. A. Leigh, “Overlapping repressor binding sites regulate expression of the Methanococcus maripaludis glnK operon,” Molecular Microbiology, vol. 75, no. 3, pp. 755–762, 2010.
[160]
U. Ermler, W. Grabarse, S. Shima, M. Goubeaud, and R. K. Thauer, “Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation,” Science, vol. 278, no. 5342, pp. 1457–1462, 1997.
[161]
J. Kahnt, B. Buchenau, F. Mahlert, M. Krüger, S. Shima, and R. K. Thauer, “Post-translational modifications in the active site region of methyl-coenzyme M reductase from methanogenic and methanotrophic archaea,” FEBS Journal, vol. 274, no. 18, pp. 4913–4921, 2007.
[162]
T. Selmer, J. Kahnt, M. Goubeaud et al., “The biosynthesis of methylated amino acids in the active site region of methyl-coenzyme M reductase,” Journal of Biological Chemistry, vol. 275, no. 6, pp. 3755–3760, 2000.
[163]
F. Yan, J. M. Lamarre, R. R？hrich et al., “RImN and Cfr are Radical SAM Enzymes Involved in Methylation of Ribosomal RNA,” Journal of the American Chemical Society, vol. 132, no. 11, pp. 3953–3964, 2010.
[164]
D. E. Graham, C. L. Bock, C. Schalk-Hihi, Z. J. Lu, and G. D. Markham, “Identification of a highly diverged class of S-adenosylmethionine synthetases in the archaea,” Journal of Biological Chemistry, vol. 275, no. 6, pp. 4055–4059, 2000.
[165]
H. P. Klenk, R. A. Clayton, J. F. Tomb et al., “The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus,” Nature, vol. 390, no. 6658, pp. 364–370, 1997.
[166]
A. W. Strittmatter, H. Liesegang, R. Rabus et al., “Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide,” Environmental Microbiology, vol. 11, no. 5, pp. 1038–1055, 2009.
[167]
L. Chistoserdova, J. A. Vorholt, R. K. Thauer, and M. E. Lidstrom, “C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic archaea,” Science, vol. 281, no. 5373, pp. 99–102, 1998.
[168]
E. G. Graf and R. K. Thauer, “Hydrogenase from Methanobacterium thermoautotrophicum, a nickel-containing enzyme,” FEBS Letters, vol. 136, no. 1, pp. 165–169, 1981.
[169]
L. Forzi and R. G. Sawers, “Maturation of [NiFe]-hydrogenases in Escherichia coli,” BioMetals, vol. 20, no. 3-4, pp. 565–578, 2007.
