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PMID: 11932238 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

The genome of M. acetivorans reveals extensive metabolic and physiological diversity.

Genome research ·Vol. 12 ·No. 4 ·2002-04-00 ·Pages 532-42

Galagan JE, Nusbaum C, Roy A, Endrizzi MG, Macdonald P, FitzHugh W, Calvo S, Engels R, Smirnov S, Atnoor D, Brown A, Allen N, Naylor J, Stange-Thomann N, DeArellano K, Johnson R, Linton L, McEwan P, McKernan K, Talamas J, Tirrell A, Ye W, Zimmer A, Barber RD, Cann I, Graham DE, Grahame DA, Guss AM, Hedderich R, Ingram-Smith C, Kuettner HC, Krzycki JA, Leigh JA, Li W, Liu J, Mukhopadhyay B, Reeve JN, Smith K, Springer TA, Umayam LA, White O, White RH, Conway de Macario E, Ferry JG, Jarrell KF, Jing H, Macario AJ, Paulsen I, Pritchett M, Sowers KR, Swanson RV, Zinder SH, Lander E, Metcalf WW, Birren B

Abstract

Methanogenesis, the biological production of methane, plays a pivotal role in the global carbon cycle and contributes significantly to global warming. The majority of methane in nature is derived from acetate. Here we report the complete genome sequence of an acetate-utilizing methanogen, Methanosarcina acetivorans C2A. Methanosarcineae are the most metabolically diverse methanogens, thrive in a broad range of environments, and are unique among the Archaea in forming complex multicellular structures. This diversity is reflected in the genome of M. acetivorans. At 5,751,492 base pairs it is by far the largest known archaeal genome. The 4524 open reading frames code for a strikingly wide and unanticipated variety of metabolic and cellular capabilities. The presence of novel methyltransferases indicates the likelihood of undiscovered natural energy sources for methanogenesis, whereas the presence of single-subunit carbon monoxide dehydrogenases raises the possibility of nonmethanogenic growth. Although motility has not been observed in any Methanosarcineae, a flagellin gene cluster and two complete chemotaxis gene clusters were identified. The availability of genetic methods, coupled with its physiological and metabolic diversity, makes M. acetivorans a powerful model organism for the study of archaeal biology. [Sequence, data, annotations and analyses are available at http://www-genome.wi.mit.edu/.]

MeSH Terms
Archaeal Proteins/genetics,physiology Carbon Monoxide/metabolism Cell Movement/genetics,physiology Euryarchaeota/metabolism Gene Expression Regulation, Archaeal/physiology Genetic Variation Genome, Archaeal Hydrogen/metabolism Membrane Proteins/genetics,physiology Methanosarcina/genetics,physiology Molecular Sequence Data Multigene Family/genetics,physiology Nitrogen Fixation/genetics,physiology Oxygen/metabolism Polysaccharides/biosynthesis,genetics Protein Biosynthesis/physiology Replication Origin/genetics,physiology Signal Transduction/genetics,physiology Transcription, Genetic
Chemicals
Archaeal Proteins Membrane Proteins Polysaccharides Carbon Monoxide Hydrogen Oxygen
Authors & Affiliations
55 authors, click to expand affiliations / ORCID
Galagan James E
Whitehead Institute Center for Genome Research, Cambridge, Massachusetts 02141, USA.
Nusbaum Chad
Roy Alice
Endrizzi Matthew G
Macdonald Pendexter
FitzHugh Will
Calvo Sarah
Engels Reinhard
Smirnov Serge
Atnoor Deven
Brown Adam
Allen Nicole
Naylor Jerome
Stange-Thomann Nicole
DeArellano Kurt
Johnson Robin
Linton Lauren
McEwan Paul
McKernan Kevin
Talamas Jessica
Tirrell Andrea
Ye Wenjuan
Zimmer Andrew
Barber Robert D
Cann Isaac
Graham David E
Grahame David A
Guss Adam M
Hedderich Reiner
Ingram-Smith Cheryl
Kuettner H Craig
Krzycki Joseph A
Leigh John A
Li Weixi
Liu Jinfeng
Mukhopadhyay Biswarup
Reeve John N
Smith Kerry
Springer Timothy A
Umayam Lowell A
White Owen
White Robert H
Conway de Macario Everly
Ferry James G
Jarrell Ken F
Jing Hua
Macario Alberto J L
Paulsen Ian
Pritchett Matthew
Sowers Kevin R
Swanson Ronald V
Zinder Steven H
Lander Eric
Metcalf William W
Birren Bruce
References (48)
48 references, click to expand
  1. Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival.
    J Bacteriol. 2001 Aug;183(15):4509-16 PMID: 11443085
  2. An anaerobic, intrachamber incubator for growth of Methanosarcina spp. on methanol-containing solid media.
    Appl Environ Microbiol. 1998 Feb;64(2):768-70 PMID: 9464421
  3. Two F420-reducing hydrogenases in methanosarcina barkeri
    Arch Microbiol. 1998 Mar;169(3):201-5 PMID: 9477253
  4. Sequence and transcript analysis of a novel Methanosarcina barkeri methyltransferase II homolog and its associated corrinoid protein homologous to methionine synthase.
    J Bacteriol. 1996 Nov;178(22):6599-607 PMID: 8932317
  5. The replication origin of archaea is finally revealed.
    Trends Biochem Sci. 2000 Nov;25(11):521-3 PMID: 11084357
  6. A novel pH2 control on the expression of flagella in the hyperthermophilic strictly hydrogenotrophic methanarchaeaon Methanococcus jannaschii.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11522-7 PMID: 11027352
  7. Sequence and transcriptional studies of five clustered flagellin genes from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1.
    FEMS Microbiol Lett. 1999 Sep 1;178(1):183-90 PMID: 10483738
  8. Disaggregation of Methanosarcina spp. and Growth as Single Cells at Elevated Osmolarity.
    Appl Environ Microbiol. 1993 Nov;59(11):3832-9 PMID: 16349092
  9. Photoactive yellow protein: a structural prototype for the three-dimensional fold of the PAS domain superfamily.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):5884-90 PMID: 9600888
  10. Conservation and variability in Archaea: protein antigens with tandem repeats encoded by a cluster of genes with common motifs in Methanosarcina mazei S-6.
    Gene. 1995 Nov 7;165(1):87-91 PMID: 7489922
  11. Integration of foreign DNA in an intergenic region of the archaeon Methanosarcina mazei without effect on transcription of adjacent genes.
    J Mol Biol. 1996 Sep 13;262(1):12-20 PMID: 8809175
  12. Context-dependent anticodon recognition by class I lysyl-tRNA synthetases.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14224-8 PMID: 11121028
  13. Is gene expression in Halobacterium NRC-1 regulated by multiple TBP and TFB transcription factors?
    Mol Microbiol. 2000 Jun;36(5):1184-5 PMID: 10844702
  14. A novel Ca2+ binding beta hairpin loop better resembles integrin sequence motifs than the EF hand.
    Cell. 2000 Aug 4;102(3):275-7 PMID: 10975518
  15. Generation of dominant selectable markers for resistance to pseudomonic acid by cloning and mutagenesis of the ileS gene from the archaeon Methanosarcina barkeri fusaro.
    J Bacteriol. 2000 May;182(9):2611-8 PMID: 10762266
  16. Directed mutagenesis and plasmid-based complementation in the methanogenic archaeon Methanosarcina acetivorans C2A demonstrated by genetic analysis of proline biosynthesis.
    J Bacteriol. 2002 Mar;184(5):1449-54 PMID: 11844777
  17. Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri.
    Eur J Biochem. 1999 Oct 1;265(1):325-35 PMID: 10491189
  18. The fla gene cluster is involved in the biogenesis of flagella in Halobacterium salinarum.
    Mol Microbiol. 2001 Aug;41(3):653-63 PMID: 11532133
  19. Mechanism and regulation of transcription in archaea.
    Curr Opin Microbiol. 2001 Apr;4(2):208-13 PMID: 11282478
  20. The molecular chaperone system and other anti-stress mechanisms in archaea.
    Front Biosci. 2001 Feb 1;6:D262-83 PMID: 11171552
  21. Expression and heat-responsive regulation of a TFIIB homologue from the archaeon Haloferax volcanii.
    Mol Microbiol. 1999 Sep;33(5):1081-92 PMID: 10476041
  22. Isolation and Characterization of a Methylotrophic Marine Methanogen, Methanococcoides methylutens gen. nov., sp. nov.
    Appl Environ Microbiol. 1983 Feb;45(2):684-90 PMID: 16346215
  23. Analyzing genomes with cumulative skew diagrams.
    Nucleic Acids Res. 1998 May 15;26(10):2286-90 PMID: 9580676
  24. Short-insert libraries as a method of problem solving in genome sequencing.
    Genome Res. 1998 May;8(5):562-6 PMID: 9582200
  25. Molecular, genetic, and biochemical characterization of the serC gene of Methanosarcina barkeri Fusaro.
    J Bacteriol. 1996 Oct;178(19):5797-802 PMID: 8824630
  26. Optimized multiplex PCR: efficiently closing a whole-genome shotgun sequencing project.
    Genomics. 1999 Dec 15;62(3):500-7 PMID: 10644449
  27. Association of hydrogen metabolism with unitrophic or mixotrophic growth of Methanosarcina barkeri on carbon monoxide.
    J Bacteriol. 1984 Apr;158(1):373-5 PMID: 6715282
  28. Genome sequence of Halobacterium species NRC-1.
    Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12176-81 PMID: 11016950
  29. Aerobic regulation of cytochrome d oxidase (cydAB) operon expression in Escherichia coli: roles of Fnr and ArcA in repression and activation.
    Mol Microbiol. 1997 Aug;25(3):605-15 PMID: 9302022
  30. Improved microbial gene identification with GLIMMER.
    Nucleic Acids Res. 1999 Dec 1;27(23):4636-41 PMID: 10556321
  31. A genetic system for Archaea of the genus Methanosarcina: liposome-mediated transformation and construction of shuttle vectors.
    Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2626-31 PMID: 9122246
  32. In vivo transposon mutagenesis of the methanogenic archaeon Methanosarcina acetivorans C2A using a modified version of the insect mariner-family transposable element Himar1.
    Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9665-70 PMID: 10920201
  33. Immunochemical differences among Methanosarcina mazei S-6 morphologic forms.
    J Bacteriol. 1992 Jul;174(14):4683-8 PMID: 1624456
  34. Cell wall polymers in Archaea (Archaebacteria).
    Cell Mol Life Sci. 1998 Apr;54(4):305-8 PMID: 9614965
  35. Posttranslational processing of Methanococcus voltae preflagellin by preflagellin peptidases of M. voltae and other methanogens.
    J Bacteriol. 2000 Feb;182(3):855-8 PMID: 10633127
  36. PAS: a multifunctional domain family comes to light.
    Curr Biol. 1997 Nov 1;7(11):R674-7 PMID: 9382818
  37. An Escherichia coli hydrogenase-3-type hydrogenase in methanogenic archaea.
    Eur J Biochem. 1998 Mar 15;252(3):467-76 PMID: 9546662
  38. Topology prediction for helical transmembrane proteins at 86% accuracy.
    Protein Sci. 1996 Aug;5(8):1704-18 PMID: 8844859
  39. Methanosarcina acetivorans sp. nov., an Acetotrophic Methane-Producing Bacterium Isolated from Marine Sediments.
    Appl Environ Microbiol. 1984 May;47(5):971-8 PMID: 16346552
  40. The trimethylamine methyltransferase gene and multiple dimethylamine methyltransferase genes of Methanosarcina barkeri contain in-frame and read-through amber codons.
    J Bacteriol. 2000 May;182(9):2520-9 PMID: 10762254
  41. Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection.
    J Bacteriol. 2001 Apr;183(8):2454-62 PMID: 11274104
  42. The Comprehensive Microbial Resource.
    Nucleic Acids Res. 2001 Jan 1;29(1):123-5 PMID: 11125067
  43. Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3.
    DNA Res. 1998 Apr 30;5(2):55-76 PMID: 9679194
  44. Cloning and sequencing of a multigene family encoding the flagellins of Methanococcus voltae.
    J Bacteriol. 1991 Nov;173(22):7113-25 PMID: 1718944
  45. TIGRFAMs: a protein family resource for the functional identification of proteins.
    Nucleic Acids Res. 2001 Jan 1;29(1):41-3 PMID: 11125044
  46. The Pfam protein families database.
    Nucleic Acids Res. 2000 Jan 1;28(1):263-6 PMID: 10592242
  47. The amber codon in the gene encoding the monomethylamine methyltransferase isolated from Methanosarcina barkeri is translated as a sense codon.
    J Biol Chem. 2001 Sep 7;276(36):34252-8 PMID: 11435424
  48. Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis.
    J Bacteriol. 1993 Oct;175(19):6276-86 PMID: 8407800
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
Published
2002-04-00
Pages
532-42
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC187521
Subset
IM
Databases
GENBANK
AE010299
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