Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Borrel, Guillaume ^a,b   Parisot, Nicolas ^a,c   Harris, Hugh M B ^b   Peyretaillade, Eric ^a   Gaci, Nadia ^a   Tottey, William ^a   Bardot, Olivier ^a   Raymann, Kasie ^d,e   Gribaldo, Simonetta ^d,e   Peyret, Pierre ^a   O'Toole, Paul W ^b   Brugère, Jean Franҫois ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c CNRS   (France)

^d Unite de Biologie Mole culaire du Ge ne chez les Extre mophiles   (France)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

Archaea; CRISPR; Energy conservation; Genome streamlining; H2 dependent methylotrophic methanogenesis; Methanomassiliicoccales; Methanomassiliicoccus; Methanomethylophilus; Origin of replication (ORI) binding (ORB) motif; Pyrrolysine Pyl

Indexed keywords

LYSINE DERIVATIVE; PYRROLYSINE; RIBOSOME RNA; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; ARCHAEAL RNA; LYSINE; STOP CODON;

ARTICLE; BACTERIAL GENOME; CANDIDATUS METHANOMASSILIICOCCUS INTESTINALIS; CANDIDATUS METHANOMETHYLOPHILUS ALVUS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CODON USAGE; COMPARATIVE STUDY; ENERGY CONSERVATION; EURYARCHAEOTA; EVOLUTIONARY ADAPTATION; GASTROINTESTINAL TRACT; GENOMICS; METHANOGENIC ARCHAEON; METHANOMASSILIICOCCALES; METHANOMASSILIICOCCUS LUMINYENSIS; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; RNA TRANSLATION; THERMOPLASMATALES; UNINDEXED SEQUENCE; ANALOGS AND DERIVATIVES; ARCHAEAL GENOME; BIOSYNTHESIS; DNA REPLICATION ORIGIN; ENERGY METABOLISM; GENETICS; MOLECULAR GENETICS; PHYLOGENY; STOP CODON;

THERMOPLASMATALES;

ARCHAEAL PROTEINS; BIOSYNTHETIC PATHWAYS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CODON, TERMINATOR; ENERGY METABOLISM; GENOME, ARCHAEAL; LYSINE; MOLECULAR SEQUENCE DATA; PHYLOGENY; REPLICATION ORIGIN; RNA, ARCHAEAL; RNA, RIBOSOMAL; THERMOPLASMALES;

EID: 84906924522     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-679     Document Type: Article

References (117)

1. Tajima K, Nagamine T, Matsui H, Nakamura M, Aminov RI. Phylogenetic analysis of archaeal 16S rRNA libraries from the rumen suggests the existence of a novel group of archaea not associated with known methanogens. FEMS Microbiol Lett 2001, 200(1):67-72.
2. Wright A-DG, Williams AJ, Winder B, Christophersen CT, Rodgers SL, Smith KD. Molecular diversity of rumen methanogens from sheep in Western Australia. Appl Environ Microb 2004, 70(3):1263-1270.
3. Janssen PH, Kirs M. Structure of the archaeal community of the rumen. Appl Environ Microb 2008, 74(12):3619-3625.
4. Mihajlovski A, Alric M, Bruge`re J-F. A putative new order of methanogenic Archaea inhabiting the human gut, as revealed by molecular analyses of the mcrA gene. Res Microbiol 2008, 159(7):516-521.
5. Mihajlovski A, Dore´ J, Levenez F, Alric M, Bruge`re JF. Molecular evaluation of the human gut methanogenic archaeal microbiota reveals an age-associated increase of the diversity. Environ Microbiol Rep 2010, 2(2):272-280.
6. Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M. Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 2012, 62(Pt 8):1902-1907.
7. Borrel G, Harris HM, Tottey W, Mihajlovski A, Parisot N, Peyretaillade E, Peyret P, Gribaldo S, O'Toole PW, Bruge`re JF. Genome sequence of "Candidatus Methanomethylophilus alvus" Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J Bacteriol 2012, 194(24):6944-6945.
8. Borrel G, Harris HM, Parisot N, Gaci N, Tottey W, Mihajlovski A, Deane J, Gribaldo S, Bardot O, Peyretaillade E. Genome sequence of "Candidatus Methanomassiliicoccus intestinalis" Issoire-Mx1, a third Thermoplasmatales-related methanogenic archaeon from human feces. Genome Announc 2013, 1(4):e00453-00413.
9. Paul K, Nonoh JO, Mikulski L, Brune A. "Methanoplasmatales", Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microb 2012, 78(23):8245-8253.
10. Iino T, Tamaki H, Tamazawa S, Ueno Y, Ohkuma M, Suzuki K, Igarashi Y, Haruta S. Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a Methanogenic Lineage of the Class Thermoplasmata. Microbes Environ/JSME 2013, 28(2):244-250.
11. Hedderich R, Whitman WB. Physiology and biochemistry of the methane-producing Archaea. The prokaryotes 2006, 1050-1079. New York: Springer.
12. Oren A, Garrity GM. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2013, 63(11):3931-3934.
13. Huang XD, Tan HY, Long R, Liang JB, Wright A-DG. Comparison of methanogen diversity of yak (Bos grunniens) and cattle (Bos taurus) from the Qinghai-Tibetan plateau, China. BMC Microbiol 2012, 12(1):237.
14. Wright A-DG, Auckland CH, Lynn DH. Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Appl Environ Microb 2007, 73(13):4206-4210.
15. Wright A-DG, Toovey AF, Pimm CL. Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveal more uncultured novel archaea. Anaerobe 2006, 12(3):134-139.
16. Borrel G, O'Toole PW, Harris HM, Peyret P, Bruge`re J-F, Gribaldo S. Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis. Genome Biol Evol 2013, 5(10):1769-1780.
17. Poulsen M, Schwab C, Jensen BB, Engberg RM, Spang A, Canibe N, Hojberg O, Milinovich G, Fragner L, Schleper C, Weckwerth W, Lund P, Schramm A, Urich T. Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nat Commun 2013, 4:1428.
18. Gorlas A, Robert C, Gimenez G, Drancourt M, Raoult D. Complete genome sequence of Methanomassiliicoccus luminyensis, the largest genome of a human-associated Archaea species. J Bacteriol 2012, 194(17):4745-4745.
19. Gaci N, Borrel G, Tottey W, O'Toole PW, Bruge`re JF. Archaea from the human gut: the new beginning of an old story. World J Gastroenterol in press.
20. Bruge`re JF, Borrel G, Gaci N, Tottey W, O'Toole PW, Malpuech-Bruge`re C. Archaebiotics: proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease. Gut Microbes 2014, 5(1):6.
21. Mackay RJ, McEntyre CJ, Henderson C, Lever M, George PM. Trimethylaminuria: causes and diagnosis of a socially distressing condition. Clin Biochem Rev 2011, 32(1):33.
22. Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, DuGar B, Feldstein AE, Britt EB, Fu X, Chung Y-M. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011, 472(7341):57-63.
23. Srinivasan G, James CM, Krzycki JA. Pyrrolysine encoded by UAG in Archaea: charging of a UAG-decoding specialized tRNA. Science 2002, 296(5572):1459-1462.
24. Krzycki JA. Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases. Curr Opin Chem Biol 2004, 8(5):484-491.
25. Borrel G, Gaci N, Peyret P, O'Toole PW, Gribaldo S, Bruge`re J-F. Unique characteristics of the pyrrolysine system in the 7th order of methanogens: implications for the evolution of a genetic code expansion cassette. Archaea 2014, 2014:374146.
26. Sheppard K, Yuan J, Hohn MJ, Jester B, Devine KM, So¨ll D. From one amino acid to another: tRNA-dependent amino acid biosynthesis. Nucleic Acids Res 2008, 36(6):1813-1825.
27. Ree HK, Zimmermann RA. Organization and expression of the 16S, 23S and 5S ribosomal RNA genes from the archaebacterium Thermoplasma acidophilum. Nucleic Acids Res 1990, 18(15):4471-4478.
28. Ciesielski S, Bulkowska K, Dabrowska D, Kaczmarczyk D, Kowal P, Mozejko J. Ribosomal intergenic spacer analysis as a tool for monitoring methanogenic archaea changes in an anaerobic digester. Curr Microbiol 2013,
29. Dufresne A, Garczarek L, Partensky F. Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 2005, 6(2):R14.
30. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315(5819):1709-1712.
31. Fischer S, Maier LK, Stoll B, Brendel J, Fischer E, Pfeiffer F, Dyall-Smith M, Marchfelder A. An archaeal immune system can detect multiple protospacer adjacent motifs (PAMs) to target invader DNA. J Biol Chem 2012, 287(40):33351-33363.
32. Sorek R, Kunin V, Hugenholtz P. CRISPR-a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 2008, 6(3):181-186.
33. Jansen R, Embden JD, Gaastra W, Schouls LM. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 2002, 43(6):1565-1575.
34. Lange SJ, Alkhnbashi OS, Rose D, Will S, Backofen R. CRISPRmap: an automated classification of repeat conservation in prokaryotic adaptive immune systems. Nucleic Acids Res 2013, 41(17):8034-8044.
35. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, van der Oost J, Koonin EV. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 2011, 9(6):467-477.
36. Stevenson DM, Weimer PJ. Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl Microbiol Biotechnol 2007, 75(1):165-174.
37. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, et al. Enterotypes of the human gut microbiome. Nature 2011, 473(7346):174-180.
38. Prangishvili D, Forterre P, Garrett RA. Viruses of the Archaea: a unifying view. Nat Rev Microbiol 2006, 4(11):837-848.
39. Prangishvili D, Garrett RA, Koonin EV. Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res 2006, 117(1):52-67.
40. Pelve EA, Martens-Habbena W, Stahl DA, Bernander R. Mapping of active replication origins in vivo in thaum-and euryarchaeal replicons. Mol Microbiol 2013, 90(3):538-550.
41. Raymann K, Forterre P, Brochier-Armanet C, Gribaldo S. Global phylogenomic analysis disentangles the complex evolutionary history of DNA replication in Archaea. Genome Biol Evol 2014, 6(1):192-212.
42. Forterre P, Gribaldo S, Gadelle D, Serre M-C. Origin and evolution of DNA topoisomerases. Biochimie 2007, 89(4):427-446.
43. Brochier-Armanet C, Forterre P, Gribaldo S. Phylogeny and evolution of the Archaea: one hundred genomes later. Curr Opin Microbiol 2011, 14(3):274-281.
44. White MF, Bell SD. Holding it together: chromatin in the Archaea. Trends Genet 2002, 18(12):621-626.
45. Makarova KS, Sorokin AV, Novichkov PS, Wolf YI, Koonin EV. Clusters of orthologous genes for 41 archaeal genomes and implications for evolutionary genomics of archaea. Biol Direct 2007, 2:33.
46. Huynen MA, Dandekar T, Bork P. Variation and evolution of the citric-acid cycle: a genomic perspective. Trends Microbiol 1999, 7(7):281-291.
47. Brown AM, Hoopes SL, White RH, Sarisky CA. Purine biosynthesis in archaea: variations on a theme. Biol Direct 2011, 6(1):63.
48. Sakai S, Takaki Y, Shimamura S, Sekine M, Tajima T, Kosugi H, Ichikawa N, Tasumi E, Hiraki AT, Shimizu A, Kato Y, Nishiko R, Mori K, Fujita N, Imachi H, Takai K. Genome sequence of a mesophilic hydrogenotrophic methanogen Methanocella paludicola, the first cultivated representative of the order Methanocellales. PLoS One 2011, 6(7):e22898.
49. Erkel C, Kube M, Reinhardt R, Liesack W. Genome of Rice Cluster I archaea-the key methane producers in the rice rhizosphere. Science 2006, 313(5785):370-372.
50. Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC genomics 2012, 13:162.
51. Lai MC, Hong TY, Gunsalus RP. Glycine betaine transport in the obligate halophilic archaeon Methanohalophilus portucalensis. J Bacteriol 2000, 182(17):5020-5024.
52. Roessler M, Pfluger K, Flach H, Lienard T, Gottschalk G, Muller V. Identification of a salt-induced primary transporter for glycine betaine in the methanogen Methanosarcina mazei Go1. Appl Environ Microbiol 2002, 68(5):2133-2139.
53. Fricke WF, Seedorf H, Henne A, Kru¨er M, Liesegang H, Hedderich R, Gottschalk G, Thauer RK. The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis. J Bacteriol 2006, 188(2):642-658.
54. Samuel BS, Hansen EE, Manchester JK, Coutinho PM, Henrissat B, Fulton R, Latreille P, Kim K, Wilson RK, Gordon JI. Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut. Proc Natl Acad Sci U S A 2007, 104(25):10643-10648.
55. Mittl PR, Schneider-Brachert W. Sel1-like repeat proteins in signal transduction. Cell Signal 2007, 19(1):20-31.
56. Tallant TC, Paul L, Krzycki JA. The MtsA subunit of the methylthiol: coenzyme M methyltransferase of Methanosarcina barkeri catalyses both half-reactions of corrinoid-dependent dimethylsulfide: coenzyme M methyl transfer. J Biol Chem 2001, 276(6):4485-4493.
57. Kaster A-K, Goenrich M, Seedorf H, Liesegang H, Wollherr A, Gottschalk G, Thauer RK. More than 200 genes required for methane formation from H 2 and CO 2 and energy conservation are present in Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus. Archaea 2011, 2011:973848.
58. Rouvie`re PE, Escalante-Semerena JC, Wolfe RS. Component A2 of the methylcoenzyme M methylreductase system from Methanobacterium thermoautotrophicum. J Bacteriol 1985, 162(1):61-66.
59. Raymond J, Siefert JL, Staples CR, Blankenship RE. The natural history of nitrogen fixation. Mol Biol Evol 2004, 21(3):541-554.
60. Shin DH. Preliminary structural studies on the MtxX protein from Methanococcus jannaschii. Acta Crystallogr Sect F: Struct Biol Cryst Commun 2008, 64(4):300-303.
61. Graham DE, Taylor SM, Wolf RZ, Namboori SC. Convergent evolution of coenzyme M biosynthesis in the Methanosarcinales: cysteate synthase evolved from an ancestral threonine synthase. Biochem J 2009, 424(3):467-478.
62. Graham DE, Graupner M, Xu H, White RH. Identification of coenzyme M biosynthetic 2-phosphosulfolactate phosphatase: a member of a new class of Mg(2+)-dependent acid phosphatases. Eur J Biochem 2001, 268(19):5176-5188.
63. Graham DE, Xu H, White RH. Identification of coenzyme M biosynthetic phosphosulfolactate synthase: a new family of sulfonate-biosynthesizing enzymes. J Biol Chem 2002, 277(16):13421-13429.
64. Graupner M, Xu H, White RH. Identification of an archaeal 2-hydroxy acid dehydrogenase catalyzing reactions involved in coenzyme biosynthesis in methanoarchaea. J Bacteriol 2000, 182(13):3688-3692.
65. Schlegel K, Muller V. Evolution of Na and H bioenergetics in methanogenic archaea. Biochem Soc T 2013, 41(1):421-426.
66. Anderson I, Ulrich LE, Lupa B, Susanti D, Porat I, Hooper SD, Lykidis A, Sieprawska-Lupa M, Dharmarajan L, Goltsman E. Genomic characterization of methanomicrobiales reveals three classes of methanogens. PLoS One 2009, 4(6):e5797.
67. Kaster A-K, Moll J, Parey K, Thauer RK. Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. Proc Natl Acad Sci U S A 2011, 108(7):2981-2986.
68. Thauer RK, Kaster A-K, Seedorf H, Buckel W, Hedderich R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 2008, 6(8):579-591.
69. Moparthi VK, Ha¨gerha¨ll C. The evolution of respiratory chain complex I from a smaller last common ancestor consisting of 11 protein subunits. J Mol Evol 2011, 72(5-6):484-497.
70. Ba¨umer S, Ide T, Jacobi C, Johann A, Gottschalk G, Deppenmeier U. The F420H2 dehydrogenase from Methanosarcina mazei is a redox-driven proton pump closely related to NADH dehydrogenases. J Biol Chem 2000, 275(24):17968-17973.
71. Welte C, Deppenmeier U. Membrane-bound electron transport in Methanosaeta thermophila. J Bacteriol 2011, 193(11):2868-2870.
72. Tran QH, Bongaerts J, Vlad D, Unden G. Requirement for the proton-pumping NADH dehydrogenase i of Escherichia coli in respiration of NADH to fumarate and its bioenergetic implications. Eur J Biochem 1997, 244(1):155-160.
73. Welte C, Kra¨tzer C, Deppenmeier U. Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei. FEBS J 2010, 277(16):3396-3403.
74. Meuer J, Kuettner HC, Zhang JK, Hedderich R, Metcalf WW. Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci U S A 2002, 99(8):5632-5637.
75. Ba¨umer S, Lentes S, Gottschalk G, Deppenmeier U. Identification and analysis of proton-translocating pyrophosphatases in the methanogenic archaeon Methanosarcina mazei. Archaea 2002, 1(1):1.
76. Baykov AA, Malinen AM, Luoto HH, Lahti R. Pyrophosphate-fueled Na + and H + transport in prokaryotes. Microbiol Mol Biol R 2013, 77(2):267-276.
77. Prat L, Heinemann IU, Aerni HR, Rinehart J, O'Donoghue P, Soll D. Carbon source-dependent expansion of the genetic code in bacteria. Proc Natl Acad Sci U S A 2012, 109(51):21070-21075.
78. Gaston MA, Jiang R, Krzycki JA. Functional context, biosynthesis, and genetic encoding of pyrrolysine. Curr Opin Microbiol 2011, 14(3):342-349.
79. Heinemann IU, O'Donoghue P, Madinger C, Benner J, Randau L, Noren CJ, Soll D. The appearance of pyrrolysine in tRNAHis guanylyltransferase by neutral evolution. Proc Natl Acad Sci U S A 2009, 106(50):21103-21108.
80. Krzycki JA. Translation of UAG as Pyrrolysine. Recoding: Expansion of Decoding Rules Enriches Gene Expression 2010, 53-77. New York: Springer.
81. Longstaff DG, Blight SK, Zhang L, Green-Church KB, Krzycki JA. In vivo contextual requirements for UAG translation as pyrrolysine. Mol Microbiol 2007, 63(1):229-241.
82. Veit K, Ehlers C, Schmitz RA. Effects of nitrogen and carbon sources on transcription of soluble methyltransferases in Methanosarcina mazei strain Go¨1. J Bacteriol 2005, 187(17):6147-6154.
83. Bailey S, Rycroft A, Elliott J. Production of amines in equine cecal contents in an in vitro model of carbohydrate overload. J Anim Sci 2002, 80(10):2656-2662.
84. Smith E, Macfarlane G. Studies on amine production in the human colon: enumeration of amine forming bacteria and physiological effects of carbohydrate and pH. Anaerobe 1996, 2(5):285-297.
85. Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L. Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 2013, 19(5):576-585.
86. Mitchell AD, Chappell A, Knox K. Metabolism of betaine in the ruminant. J Anim Sci 1979, 49(3):764-774.
87. Neill AR, Grime DW, Dawson R. Conversion of choline methyl groups through trimethylamine into methane in the rumen. Biochem J 1978, 170:529-535.
88. Benstead J, King G, Williams H. Methanol promotes atmospheric methane oxidation by methanotrophic cultures and soils. Appl Environ Microb 1998, 64(3):1091-1098.
89. Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM. The minimal gene complement of Mycoplasma genitalium. Science 1995, 270(5235):397-404.
90. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS Nat 2000, 407(6800):81-86.
91. Waters E, Hohn MJ, Ahel I, Graham DE, Adams MD, Barnstead M, Beeson KY, Bibbs L, Bolanos R, Keller M. The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc Natl Acad Sci U S A 2003, 100(22):12984-12988.
92. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen G, Olson R, Osterman A, Overbeek R, McNeil L, Paarmann D, Paczian T, Parrello B, Pusch G, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75.
93. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007, 23(6):673-679.
94. Bairoch A, Boeckmann B. The SWISS-PROT protein sequence data bank. Nucleic Acids Res 1991, 19(Suppl):2247.
95. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR. Rfam: updates to the RNA families database. Nucleic Acids Res 2009, 37(suppl 1):D136-D140.
96. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 2005, 33(Web Server issue):W686-W689.
97. Taquist H, Cui Y, Ardell DH. TFAM 1.0: an online tRNA function classifier. Nucleic Acids Res 2007, 35(Web Server issue):W350-W353.
98. Laslett D, Canback B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 2004, 32(1):11-16.
99. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
100. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007, 35(Web Server issue):W52-W57.
101. Grissa I, Vergnaud G, Pourcel C. CRISPRcompar: a website to compare clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2008, 36(Web Server issue):W145-W148.
102. Lange SJ, Alkhnbashi OS, Rose D, Will S, Backofen R. CRISPRmap: an automated classification of repeat conservation in prokaryotic adaptive immune systems. Nucleic Acids Res 2013, 41(17):8034-8044.
103. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res 2011, 39(Web Server issue):W347-W352.
104. Grant JR, Stothard P. The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 2008, 36(suppl 2):W181-W184.
105. Oliveros J. VENNY: an interactive tool for comparing lists with Venn Diagrams. 2007, http://bioinfogp.cnb.csic.es/tools/venny/index.html.
106. Magrane M. UniProt Knowledgebase: a hub of integrated protein data. Database 2011, 2011:bar009.
107. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007, 35(suppl 2):W182-W185.
108. Li H, Benedito V, Udvardi M, Zhao P. TransportTP: a two-phase classification approach for membrane transporter prediction and characterization. BMC Bioinform 2009, 10(1):418.
109. Ren Q, Chen K, Paulsen IT. TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels. Nucleic Acids Res 2007, 35(suppl 1):D274-D279.
110. Go¨tz S, Garci´a-Go´mez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talo´n M, Dopazo J, Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 2008, 36(10):3420-3435.
111. Johnson LS, Eddy S, Portugaly E. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinform 2010, 11(1):431.
112. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
113. Philippe H. MUST, a computer package of management utilities for sequences and trees. Nucleic Acids Res 1993, 21(22):5264-5272.
114. Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010, 10(1):210.
115. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22(21):2688-2690.
116. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Ho¨hna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012, 61(3):539-542.
117. Hofacker IL. Vienna RNA secondary structure server. Nucleic Acids Res 2003, 31(13):3429-3431.