Genome sequence of Thermofilum pendens reveals an exceptional loss of biosynthetic pathways without genome reduction

Journal of Bacteriology

Volumn 190, Issue 8, 2008, Pages 2957-2965

  Anderson, Iain ^a   Rodriguez, Jason ^b,c   Susanti, Dwi ^b,c   Porat, Iris ^d,i   Reich, Claudia ^e   Ulrich, Luke E ^f   Elkins, James G ^g   Mavromatis, Kostas ^a   Lykidis, Athanasios ^a   Kim, Edwin ^a   Thompson, Linda S ^a,h   Nolan, Matt ^a   Land, Miriam ^g   Copeland, Alex ^a   Lapidus, Alla ^a   Lucas, Susan ^a   Detter, Chris ^a,h   Zhulin, Igor B ^f   Olsen, Gary J ^e   Whitman, William ^d   Mukhopadhyay, Biswarup ^b,c   Bristow, James ^a   Kyrpides, Nikos ^a   more..

^a DOE JOINT GENOME INSTITUTE   (United States)

^b VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^f Oak Ridge National Laboratory   (United States)

^g OAK RIDGE NATIONAL LABORATORY   (United States)

^h LOS ALAMOS NATIONAL LABORATORY   (United States)

ⁱ PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; AMINO ACID; CARBOHYDRATE; CORRINOID; FORMATE DEHYDROGENASE; FORMIC ACID; HYDROGEN; METHYLAMINE; PALINDROMIC DNA; PEPTIDE; PHOSPHOTRANSFERASE; PRESENILIN; PURINE; REPETITIVE DNA; SULFUR;

ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM; BIOSYNTHESIS; CRENARCHAEOTA; ELECTRON; ENERGY; EXTRACELLULAR SPACE; FERMENTATION; GENE CLUSTER; GENE SEQUENCE; HETEROTROPH; HOUSEKEEPING GENE; HYPERTHERMOPHILIC BACTERIUM; ICELAND; INTRACELLULAR SPACE; METHANOSARCINA; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT; PARASITE; PRIORITY JOURNAL; REDUCTION KINETICS; THERMOFILUM; THERMOFILUM PENDENS; THERMOPROTEALES; THERMOPROTEUS TENAX;

ARCHAEAL PROTEINS; BASE COMPOSITION; BIOSYNTHETIC PATHWAYS; CARRIER PROTEINS; DNA, ARCHAEAL; ENVIRONMENTAL MICROBIOLOGY; GENES, ARCHAEAL; GENOME, ARCHAEAL; ICELAND; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; THERMOFILACEAE;

ARCHAEA; CRENARCHAEOTA; METHANOSARCINALES; THERMOFILUM PENDENS; THERMOPROTEALES; THERMOPROTEUS TENAX;

EID: 41949089913     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01949-07     Document Type: Article

References (64)

1. Adams, M. W. W., J. F. Holden, A. L. Menon, G. J. Schut, A. M. Grunden, C. Hou, A. M. Hutchins, F. E. Jenney, Jr., C. Kim, K. Ma, G. Pan, R. Roy, R. Sapra, S. V. Story, and M. F. J. M. Verhagen. 2001. Key role for sulfur in peptide metabolism and in regulation of three hydrogenases in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 183:716-724.
2. Badger, J. H., and G. J. Olsen. 1999. CRITICA: coding region identification tool invoking comparative analysis. Mol. Biol. Evol. 16:512-524.
3. Barrangou, R., C. Fremaux, H. Deveau, M. Richards, P. Boyaval, S. Moineau, D. A. Romero, and P. Horvath. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709-1712.
4. Bräsen, C., C. Urbanke, and P. Schönheit. 2005. A novel octameric AMP-forming acetyl-CoA synthetase from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. FEBS Lett. 579:477-482.
5. Chen, L., K. Brügger, M. Skovgaard, P. Redder, Q. She, E. Torarinsson, B. Greve, M. Awayez, A. Zibat, H.-P. Klenk, and R. A. Garrett. 2005. The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J. Bacteriol. 187:4992-4999.
6. Delcher, A. L., D. Harmon, S. Kasif, O. White, and S. L. Salzberg. 1999. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27:4636-4641.
7. Ewing, B., and P. Green. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8:186-194.
8. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175-185.
9. Finn, R. D., J. Tate, J. Mistry, P. C. Coggill, S. J. Sammut, H.-R. Hotz, G. Ceric, K. Forslund, S. R. Eddy, E. L. L. Sonnhammer, and A. Bateman. 2008. The Pfam protein families database. Nucleic Acids Res. 36:D281-D288.
10. Gordon, D., C. Abajian, and P. Green. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8:195-202.
11. Grigorenko, A. P., Y. K. Moliaka, G. I. Korovaitseva, and E. I. Rogaev. 2002. Novel class of polytopic proteins with domains associated with putative protease activity. Biochemistry (Moscow) 67:826-835.
12. Grigoriev, A. 1998. Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res. 26:2286-2290.
13. Grochowski, L. L., H. Xu, and R. H. White. 2006. Methanocaldococcus jannaschii uses a modified mevalonate pathway for biosynthesis of isopentenyl diphosphate. J. Bacteriol. 188:3192-3198.
14. Hakobyan, M., H. Sargsyan, and K. Bagramyan. 2005. Proton translocation coupled to formate oxidation in anaerobically grown fermenting Escherichia coli. Biophys. Chem. 115:55-61.
15. Hallam, S. J., K. T. Konstantinidis, N. Putnam, C. Schleper, Y. Watanabe, J. Sugahara, C. Preston, J. de la Torre, P. M. Richardson, and E. F. DeLong. 2006. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl. Acad. Sci. USA 103:18296-18301.
16. Han, C. S., and P. Chain. 2006. Finishing repeat regions automatically with Dupfinisher, p. 141-146. In H. R. Arabnia and H. Valafar (ed.), Proceedings of the 2006 International Conference on Bioinformatics and Computational Biology. CSREA Press, Las Vegas, NV.
17. Hansen, T., L. Arnfors, R. Ladenstein, and P. Schönheit. 2007. The phosphofructokinase-B (MJ0406) from Methanocaldococcus jannaschii represents a nucleoside kinase with a broad substrate specificity. Extremophiles 11:105-114.
18. Hashimoto, Y., T. Yamamoto, S. Fujiwara, M. Takagi, and T. Imanaka. 2001. Extracellular synthesis, specific recognition, and intracellular degradation of cyclomaltodextrins by the hyperthermophilic archaeon Thermococcus sp. strain B1001. J. Bacteriol. 183:5050-5057.
19. Imanaka, H., A. Yamatsu, T. Fukui, H. Atomi, and T. Imanaka. 2006. Phosphoenolpyruvate synthase plays an essential role for glycolysis in the modified Embden-Meyerhof pathway in Thermococcus kodakaraensis. Mol. Microbiol. 61:898-909.
20. Jormakka, M., B. Byrne, and S. Iwata. 2003. Formate dehydrogenase - a versatile enzyme in changing environments. Curr. Opin. Struct. Biol. 13:418-423.
21. Karlin, S., J. Mrazek, J. Ma, and L. Brocchieri. 2005. Predicted highly expressed genes in archaeal genomes. Proc. Natl. Acad. Sci. USA 102:7303-7308.
22. Kato, N., H. Yurimoto, and R. K. Thauer. 2006. The physiological role of the ribulose monophosphate pathway in bacteria and archaea. Biosci. Biotechnol. Biochem. 70:10-21.
23. Kletzin, A., and M. W. W. Adams. 1996. Molecular phylogenetic characterization of pyruvate and 2-ketoisovalerate ferredoxin oxidoreductases from Pyrococcus furiosus and pyruvate ferredoxin oxidoreductase from Thermotoga maritima. J. Bacteriol. 178:248-257.
24. Koning, S. M., M. G. L. Elferink, W. N. Konings, and A. J. M. Driessen. 2001. Cellobiose uptake in the hyperthermophilic archaeon Pyrococcus furiosus is mediated by an inducible, high-affinity ABC transporter. J. Bacteriol. 183:4979-4984.
25. Krafft, T., M. Bokranz, O. Klimmek, I. Schröder, F. Fahrenholz, E. Kojro, and A. Kröger. 1992. Cloning and nucleotide sequence of the psrA gene of Wolinella succinogenes polysulphide reductase. Eur. J. Biochem. 206:503-510.
26. Laska, S., F. Lottspeich, and A. Kletzin. 2003. Membrane-bound hydrogenase and sulfur reductase of the hyperthermophilic and acidophilic archaeon Acidianus ambivalens. Microbiology 149:2357-2371.
27. Lee, H.-S., K. R. Shockley, G. J. Schut, S. B. Conners, C. I. Montero, M. R. Johnson, C.-J. Chou, S. L. Bridger, N. Wigner, S. D. Brehm, F. E. Jenney, Jr., D. A. Comfort, R. M. Kelly, and M. W. W. Adams. 2006. Transcriptional and biochemical analysis of starch metabolism in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 188:2115-2125.
28. Letunic, I., R. R. Copley, B. Pils, S. Pinkert, J. Schultz, and P. Bork. 2006. SMART 5: domains in the context of genomes and networks. Nucleic Acids Res. 34:D257-D260.
29. Liolios, K., N. Tavernarakis, P. Hugenholtz, and N. C. Kyrpides. 2006. The Genomes On Line Database (GOLD) v. 2: a monitor of genome projects worldwide. Nucleic Acids Res. 34:D332-D334.
30. Ma, K., and M. W. W. Adams. 1994. Sulfide dehydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus: a new multifunctional enzyme involved in the reduction of elemental sulfur. J. Bacteriol. 176:6509-6517.
31. Ma, K., R. Weiss, and M. W. W. Adams. 2000. Characterization of hydrogenase II from the hyperthermophilic archaeon Pyrococcus furiosus and assessment of its role in sulfur reduction. J. Bacteriol. 182:1864-1871.
32. Mai, X., and M. W. W. Adams. 1996. Purification and characterization of two reversible and ADP-dependent acetyl coenzyme A synthetases from the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 178:5897-5903.
33. Markowitz, V. M., E. Szeto, K. Palaniappan, Y. Grechkin, K. Chu, I.-M. A. Chen, I. Dubchak, I. Anderson, A. Lykidis, K. Mavromatis, N. N. Ivanova, and N. C. Kyrpides. 2006. The integrated microbial genomes (IMG) system in 2007: data content and analysis tool extensions. Nucleic Acids Res. 34:D344-D348.
34. May, B. J., Q. Zhang, L. L. Li, M. L. Paustian, T. S. Whittam, and V. Kapur. 2001. Complete genomic sequence of Pasteurella multocida Pm70. Proc. Natl. Acad. Sci. USA 98:3460-3465.
35. Moran, N. A. 1996. Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93:2873-2878.
36. Moran, N. A., and J. J. Wernegreen. 2000. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15:321-326.
37. Mukund, S., and M. W. W. Adams. 1995. Glyceraldehyde-3-phosphate ferredoxin oxidoreductase, a novel tungsten-containing enzyme with a potential glycolytic role in the hyperthermophilic archaeon Pyrococcus furiosus. J. Biol. Chem. 270:8389-8392.
38. Müller, S., E. Liebau, R. D. Walter, and R. L. Krauth-Siegel. 2003. Thiol-based redox metabolism of protozoan parasites. Trends Parasitol. 19:320-328.
39. Nanavati, D. M., K. Thirangoon, and K. M. Noll. 2006. Several archaeal homologs of putative oligopeptide-binding proteins encoded by Thermotoga maritima bind sugars. Appl. Environ. Microbiol. 72:1336-1345.
40. Ochman, H., and N. A. Moran. 2001. Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292:1096-1099.
41. Oda, Y., K. Mino, K. Ishikawa, and M. Ataka. 2005. Three-dimensional structure of a new enzyme, O-phosphoserine sulfhydrylase, involved in L-cysteine synthesis by a hyperthermophilic archaeon, Aeropyrum pernix K1, at 2.0 Å resolution. J. Mol. Biol. 351:334-344.
42. Ortmann, A. C., B. Wiedenheft, T. Douglas, and M. Young. 2006. Hot crenarchaeal viruses reveal deep evolutionary connections. Nat. Rev. Microbiol. 4:520-528.
43. Ponting, C. P., M. Hutton, A. Nyborg, M. Baker, K. Jansen, and T. E. Golde. 2002. Identification of a novel family of presenilin homologues. Hum. Mol. Genet. 11:1037-1044.
44. 2+-, and thiol-dependent α-glucosidase. Extremophiles 4:189-200.
45. Rice, P., I. Longden, and A. Bleasby. 2000. EMBOSS: the European molecular biology open software suite. Trends Genet. 16:276-277.
46. Robinson, N. P., I. Dionne, M. Lundgren, V. L. Marsh, R. Bernander, and S. D. Bell. 2004. Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus. Cell 116:25-38.
47. Rodionov, D. A., A. G. Vitreschak, A. A. Mironov, and M. S. Gelfand. 2002. Comparative genomics of thiamin biosynthesis in prokaryotes. New genes and regulatory mechanisms. J. Biol. Chem. 277:48949-48959.
48. Roy, H., H. D. Becker, J. Reinbolt, and D. Kern. 2003. When contemporary aminoacyl-tRNA synthetases invent their cognate amino acid metabolism. Proc. Natl. Acad. Sci. USA 100:9837-9842.
49. Sakharkar, K. R., P. K. Dhar, and V. T. Chow. 2004. Genome reduction in prokaryotic obligatory intracellular parasites of humans: a comparative analysis. Int. J. Syst. Evol. Microbiol. 54:1937-1941.
50. Sato, T., H. Atomi, and T. Imanaka. 2007. Archaeal type III rubiscos function in a pathway for AMP metabolism. Science 315:1003-1006.
51. Sawers, R. G. 2005. Formate and its role in hydrogen production in Escherichia coli. Biochem. Soc. Trans. 33:42-46.
52. Schut, G. J., S. L. Bridger, and M. W. W. Adams. 2007. Insights into the metabolism of elemental sulfur by the hyperthermophilic archaeon Pyrococcus furiosus: characterization of a coenzyme A-dependent NAD(P)H sulfur oxidoreductase. J. Bacteriol. 189:4431-4441.
53. Siguier, P., J. Perochon, L. Lestrade, J. Manillon, and M. Chandler. 2006. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 34:D32-D36.
54. Tamas, I., L. Klasson, B. Canbäck, A. K. Näslund, A.-S. Eriksson, J. J. Wernegreen, J. P. Sandström, N. A. Moran, and S. G. E. Andersson. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376-2379.
55. Tatusov, R. L., N. D. Fedorova, J. D. Jackson, A. R. Jacobs, B. Kiryutin, E. V. Koonin, D. M. Krylov, R. Mazumder, S. L. Mekhedov, A. N. Nikolskaya, B. S. Rao, S. Smirnov, A. V. Sverdlov, S. Vasudevan, Y. I. Wolf, J. J. Yin, and D. A. Natale. 2003. The COG database: an updated version includes cukaryotes. BMC Bioinformatics 4:41.
56. Thomas, J. M., D. Horspool, G. Brown, V. Tcherepanov, and C. Upton. 2007. GraphDNA: a Java program for graphical display of DNA composition analyses. BMC Bioinformatics 8:21.
57. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
58. Tomb, J.-F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, K. McKenney, L. M. Fitzegerald, N. Lee, M. D. Adams, E. K. Hickey, D. E. Berg, J. D. Gocayne, T. R. Utterback, J. D. Peterson, J. M. Kelley, M. D. Cotton, J. M. Weidman, C. Fujii, C. Bowman, L. Watthey, E. Wallin, W. S. Hayes, M. Borodovsky, P. D. Karp, H. O. Smith, C. M. Fraser, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
59. Ulrich, L. E., E. V. Koonin, and I. B. Zhulin. 2005. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13:52-56.
60. Ulrich, L. E., and I. B. Zhulin. 2007. MiST: a microbial signal transduction database. Nucleic Acids Res. 35:D386-D390.
61. Uriarte, M., A. Marina, S. Ramón-Maiques, I. Fita, and V. Rubio. 1999. The carbamoyl-phosphate synthetase of Pyrococcus furiosus is enzymologically and structurally a carbamate kinase. J. Biol. Chem. 274:16295-16303.
62. Waters, E., M. J. Hohn, I. Ahel, D. E. Graham, M. D. Adams, M. Barnstead, K. Y. Beeson, L. Bibbs, R. Bolanos, M. Keller, K. Kretz, X. Lin, E. Mathur, J. Ni, M. Podar, T. Richardson, G. G. Sutton, M. Simon, D. Söll, K. O. Stetter, J. M. Short, and M. Noordewier. 2003. The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc. Natl. Acad. Sci. USA 100:12984-12988.
63. Wolfe, M. S. 2006. The gamma-secretase complex: membrane-embedded proteolytic ensemble. Biochemistry 45:7931-7939.
64. Zillig, W., A. Gierl, G. Schreiber, S. Wunderl, D. Janekovic, K. O. Stetter, and H. P. Klenk. 1983. The archaebacterium Thermofilum pendens represents a novel genus of the thermophilic, anaerobic sulfur respiring Thermoproteales. Syst. Appl. Microbiol. 4:79-87.