The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis - PubMed
- ️Invalid Date
The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis
Wolfgang F Fricke et al. J Bacteriol. 2006 Jan.
Abstract
Methanosphaera stadtmanae has the most restricted energy metabolism of all methanogenic archaea. This human intestinal inhabitant can generate methane only by reduction of methanol with H2 and is dependent on acetate as a carbon source. We report here the genome sequence of M. stadtmanae, which was found to be composed of 1,767,403 bp with an average G+C content of 28% and to harbor only 1,534 protein-encoding sequences (CDS). The genome lacks 37 CDS present in the genomes of all other methanogens. Among these are the CDS for synthesis of molybdopterin and for synthesis of the carbon monoxide dehydrogenase/acetyl-coenzyme A synthase complex, which explains why M. stadtmanae cannot reduce CO2 to methane or oxidize methanol to CO2 and why this archaeon is dependent on acetate for biosynthesis of cell components. Four sets of mtaABC genes coding for methanol:coenzyme M methyltransferases were found in the genome of M. stadtmanae. These genes exhibit homology to mta genes previously identified in Methanosarcina species. The M. stadtmanae genome also contains at least 323 CDS not present in the genomes of all other archaea. Seventy-three of these CDS exhibit high levels of homology to CDS in genomes of bacteria and eukaryotes. These 73 CDS include 12 CDS which are unusually long (>2,400 bp) with conspicuous repetitive sequence elements, 13 CDS which exhibit sequence similarity on the protein level to CDS encoding enzymes involved in the biosynthesis of cell surface antigens in bacteria, and 5 CDS which exhibit sequence similarity to the subunits of bacterial type I and III restriction-modification systems.
Figures

Circular map of the chromosome of M. stadtmanae. Rings from the outside to the inside: scale (in base pairs), protein-encoding sequences (blue or yellow), CDS with gene homologues in M. thermautotrophicus (magenta), putative highly expressed CDS (green), G+C content variation (higher values on the outside), rRNA and tRNA coding sequences (red), and cdc6 genes (black).

Metabolic pathways involved in methanol reduction to methane with H2 and in C1 unit biosynthesis from C-2 of acetate in M. stadtmanae. The genes encode the following enzymes (see text): ehb, energy-converting hydrogenase; por, pyruvate:ferredoxin oxidoreductase; ppsA, phosphoenolpyruvate synthase; eno, enolase; apg, phosphoglycerate mutase; serA, phosphoglycerate dehydrogenase; glyA, serine:H4MPT hydroxymethyl transferase; hps, hexulose phosphate synthase; fae, formaldehyde-activating enzyme; fwd, formylmethanofuran dehydrogenase; ftr, formylmethanofuran:H4MPT formyltransferase; mch, methenyl-H4MPT cyclohydrolase; fprA, F420H2 oxidase; fno, F420H2:NADP oxidoreductase; mtd, methylene-H4MPT dehydrogenase; thyA, thymidylate synthase; frh, F420-reducing hydrogenase; mer, methylene-H4MPT reductase; metE, methionine synthase; mtr, methyl-H4MPT:coenzyme M methyltransferase; mta, methanol:coenzyme M methyltransferase; mvh, non-F420-reducing hydrogenase; hdr, heterodisulfide reductase; and mrt, methyl-coenzyme M reductase. PEP, phosphoenolpyruvate; 2-PGA, 2-phosphoglycerate; 3-PGA, 3-phosphoglycerate; FBP, fructose bisphosphate; F6P, fructose-6-phosphate; Hu6P, 3-hexulose-6-phosphate; CHO-MFR, formylmethanofuran; Ru5P, ribulose-5-phosphate.

Topological model of the HdrABC/MvhADG complex catalyzing the reduction of CoM-S-S-CoB with H2 in a proton-translocating reaction in M. stadtmanae. In the model it is assumed that based on indirect evidence, HdrB is an integral membrane protein, although this is not reflected in its primary structure (see text).

Schematic representation of the 37 putative proteins encoded by the group of large CDS with a repetitive structure in M. stadtmanae. (a) General composition shared by all proteins of this group, including an N-terminal leader sequence (yellow) followed by a predicted transmembrane (TM) helix (blue) and by a variable number of repeated peptide sequences (green and red). (b) Schematic composition of the three largest proteins of this group (Msp0762 protein, 3,357 amino acids [aa]; Msp0568 protein, 2,980 aa; Msp0597 protein, 2,469 aa). Two of these, the Msp0568 and Msp0597 proteins, are unique to M. stadtmanae; only the Msp0762 protein exhibits homology to bacterial proteins (Table 4). The short leader sequence is Lys and Asn rich, typically having the form MKNK. At least one copy of a short sequence motif is found at the C terminus of all proteins in this group [G(K/R)XXXKXNGRT]. Sequence variations of repetitive peptide sequences are indicated by green. Repetitive peptides of different large CDS do not necessarily have the same sequence.
Similar articles
-
Tungsten-enhanced growth of Methanosphaera stadtmanae.
Dridi B, Khelaifia S, Fardeau ML, Ollivier B, Drancourt M. Dridi B, et al. BMC Res Notes. 2012 May 15;5:238. doi: 10.1186/1756-0500-5-238. BMC Res Notes. 2012. PMID: 22587398 Free PMC article.
-
Kaster AK, Goenrich M, Seedorf H, Liesegang H, Wollherr A, Gottschalk G, Thauer RK. Kaster AK, et al. Archaea. 2011;2011:973848. doi: 10.1155/2011/973848. Epub 2011 Apr 27. Archaea. 2011. PMID: 21559116 Free PMC article.
-
The bioenergetics of methanogenesis.
Daniels L, Sparling R, Sprott GD. Daniels L, et al. Biochim Biophys Acta. 1984 Sep 6;768(2):113-63. doi: 10.1016/0304-4173(84)90002-8. Biochim Biophys Acta. 1984. PMID: 6236847 Review.
-
Enzymology of one-carbon metabolism in methanogenic pathways.
Ferry JG. Ferry JG. FEMS Microbiol Rev. 1999 Jan;23(1):13-38. doi: 10.1111/j.1574-6976.1999.tb00390.x. FEMS Microbiol Rev. 1999. PMID: 10077852 Review.
Cited by
-
Gut and root microbiota commonalities.
Ramírez-Puebla ST, Servín-Garcidueñas LE, Jiménez-Marín B, Bolaños LM, Rosenblueth M, Martínez J, Rogel MA, Ormeño-Orrillo E, Martínez-Romero E. Ramírez-Puebla ST, et al. Appl Environ Microbiol. 2013 Jan;79(1):2-9. doi: 10.1128/AEM.02553-12. Epub 2012 Oct 26. Appl Environ Microbiol. 2013. PMID: 23104406 Free PMC article. Review.
-
Sun X, Henderson G, Cox F, Molano G, Harrison SJ, Luo D, Janssen PH, Pacheco D. Sun X, et al. PLoS One. 2015 Mar 24;10(3):e0119697. doi: 10.1371/journal.pone.0119697. eCollection 2015. PLoS One. 2015. PMID: 25803688 Free PMC article.
-
Sorokin DY, Merkel AY, Abbas B, Makarova KS, Rijpstra WIC, Koenen M, Sinninghe Damsté JS, Galinski EA, Koonin EV, van Loosdrecht MCM. Sorokin DY, et al. Int J Syst Evol Microbiol. 2018 Jul;68(7):2199-2208. doi: 10.1099/ijsem.0.002810. Epub 2018 May 29. Int J Syst Evol Microbiol. 2018. PMID: 29781801 Free PMC article.
-
Effects of antimicrobial peptides on methanogenic archaea.
Bang C, Schilhabel A, Weidenbach K, Kopp A, Goldmann T, Gutsmann T, Schmitz RA. Bang C, et al. Antimicrob Agents Chemother. 2012 Aug;56(8):4123-30. doi: 10.1128/AAC.00661-12. Epub 2012 May 14. Antimicrob Agents Chemother. 2012. PMID: 22585226 Free PMC article.
-
Tungsten-enhanced growth of Methanosphaera stadtmanae.
Dridi B, Khelaifia S, Fardeau ML, Ollivier B, Drancourt M. Dridi B, et al. BMC Res Notes. 2012 May 15;5:238. doi: 10.1186/1756-0500-5-238. BMC Res Notes. 2012. PMID: 22587398 Free PMC article.
References
-
- Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410. - PubMed
-
- Backhed, F., R. E. Ley, J. L. Sonnenburg, D. A. Peterson, and J. I. Gordon. 2005. Host-bacterial mutualism in the human intestine. Science 307:1915-1920. - PubMed
-
- Baliga, N. S., R. Bonneau, M. T. Facciotti, M. Pan, G. Glusman, E. W. Deutsch, P. Shannon, Y. L. Chiu, R. R. Gan, P. L. Hung, S. V. Date, E. Marcotte, L. Hood, and W. V. Ng. 2004. Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res. 14:2221-2234. - PMC - PubMed
-
- Bank, S., B. Yan, and T. L. Miller. 1996. Solid C13 CPMAS NMR spectroscopy studies of biosynthesis in whole cells of Methanosphaera stadtmanae. Solid State Nucl. Mag. Reson. 7:253-261. - PubMed
-
- Bott, M. H., B. Eikmanns, and R. K. Thauer. 1985. Defective formation and/or utilization of carbon-monoxide in H2Co2 fermenting methanogens dependent on acetate as carbon source. Arch. Microbiol. 143:266-269.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases