Antonie van Leeuwenhoek

, Volume 99, Issue 2, pp 133–157 | Cite as

Molecular signatures for the Crenarchaeota and the Thaumarchaeota

Review Paper

Abstract

Crenarchaeotes found in mesophilic marine environments were recently placed into a new phylum of Archaea called the Thaumarchaeota. However, very few molecular characteristics of this new phylum are currently known which can be used to distinguish them from the Crenarchaeota. In addition, their relationships to deep-branching archaeal lineages are unclear. We report here detailed analyses of protein sequences from Crenarchaeota and Thaumarchaeota that have identified many conserved signature indels (CSIs) and signature proteins (SPs) (i.e., proteins for which all significant blast hits are from these groups) that are specific for these archaeal groups. Of the identified signatures 6 CSIs and 13 SPs are specific for the Crenarchaeota phylum; 6 CSIs and >250 SPs are uniquely found in various Thaumarchaeota (viz. Cenarchaeum symbiosum, Nitrosopumilus maritimus and a number of uncultured marine crenarchaeotes) and 3 CSIs and ~10 SPs are found in both Thaumarchaeota and Crenarchaeota species. Some of the molecular signatures are also present in Korarchaeumcryptofilum, which forms the independent phylum Korarchaeota. Although some of these molecular signatures suggest a distant shared ancestry between Thaumarchaeota and Crenarchaeota, our identification of large numbers of Thaumarchaeota-specific proteins and their deep branching between the Crenarchaeota and Euryarchaeota phyla in phylogenetic trees shows that they are distinct from both Crenarchaeota and Euryarchaeota in both genetic and phylogenetic terms. These observations support the placement of marine mesophilic archaea into the separate phylum Thaumarchaeota. Additionally, many CSIs and SPs have been found that are specific for different orders within Crenarchaeota (viz. Sulfolobales—3 CSIs and 169 SPs, Thermoproteales—5 CSIs and 25 SPs, Desulfurococcales—4 SPs, and Sulfolobales and Desulfurococcales—2 CSIs and 18 SPs). The signatures described here provide novel means for distinguishing the Crenarchaeota and the Thaumarchaeota and for the classification of related and novel species in different environments. Functional studies on these signature proteins could lead to discovery of novel biochemical properties that are unique to these groups of archaea.

Keywords

Mesophilic crenarchaea Thaumarchaeota Crenarchaeota Archaeal phylogeny Conserved signature indels Signature proteins Korarchaeum Sulfolobales Thermoproteales Desulfurococcales 

Supplementary material

10482_2010_9488_MOESM1_ESM.pdf (382 kb)
Supplementary material 1 (PDF 381 kb)

References

  1. Anderson I, Rodriguez J, Susanti D et al (2008) Genome sequence of Thermofilum pendens reveals an exceptional loss of biosynthetic pathways without genome reduction. J Bacteriol 190:2957–2965CrossRefPubMedGoogle Scholar
  2. Anderson IJ, Dharmarajan L, Rodriguez J et al (2009) The complete genome sequence of Staphylothermus marinus reveals differences in sulfur metabolism among heterotrophic Crenarchaeota. BMC Genomics 10:145CrossRefPubMedGoogle Scholar
  3. Baldauf SL, Palmer JD (1993) Animals and fungi are each other’s closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci USA 90:11558–11562CrossRefPubMedGoogle Scholar
  4. Bapteste E, Philippe H (2002) The potential value of indels as phylogenetic markers: position of trichomonads as a case study. Mol Biol Evol 19:972–977PubMedGoogle Scholar
  5. Bapteste E, Brochier C, Boucher Y (2005) Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. Archaea 1:353–363CrossRefPubMedGoogle Scholar
  6. Barns SM, Delwiche CF, Palmer JD, Pace NR (1996) Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc Natl Acad Sci USA 93:9188–9193CrossRefPubMedGoogle Scholar
  7. Brochier C, Forterre P, Gribaldo S (2005a) An emerging phylogenetic core of Archaea: phylogenies of transcription and translation machineries converge following addition of new genome sequences. BMC Evol Biol 5:36CrossRefPubMedGoogle Scholar
  8. Brochier C, Gribaldo S, Zivanovic Y, Confalonieri F, Forterre P (2005b) Nanoarchaea: representatives of a novel archaeal phylum or a fast-evolving euryarchaeal lineage related to Thermococcales? Genome Biol 6:R42CrossRefPubMedGoogle Scholar
  9. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008a) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252CrossRefPubMedGoogle Scholar
  10. Brochier-Armanet C, Gribaldo S, Forterre P (2008b) A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya. Biol Direct 3:54CrossRefPubMedGoogle Scholar
  11. Brockl G, Berchtold M, Behr M, Konig H (1992) Sequence of the 5-aminolevulinic acid dehydratase-encoding gene from the hyperthermophilic methanogen, Methanothermus sociabilis. Gene 119:151–152CrossRefPubMedGoogle Scholar
  12. Burggraf S, Huber H, Stetter KO (1997) Reclassification of the crenarchaeal orders and families in accordance with 16S rRNA sequence data. Int J Syst Bacteriol 47:657–660CrossRefPubMedGoogle Scholar
  13. Cacciapuoti G, Bertoldo C, Brio A, Zappia V, Porcelli M (2003) Purification and characterization of 5′-methylthioadenosine phosphorylase from the hyperthermophilic archaeon Pyrococcus furiosus: substrate specificity and primary structure analysis. Extremophiles 7:159–168PubMedGoogle Scholar
  14. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287CrossRefPubMedGoogle Scholar
  15. Daubin V, Gouy M, Perriere G (2002) A phylogenomic approach to bacterial phylogeny: evidence of a core of genes sharing a common history. Genome Res 12:1080–1090CrossRefPubMedGoogle Scholar
  16. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689CrossRefPubMedGoogle Scholar
  17. DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50:470–478CrossRefPubMedGoogle Scholar
  18. Delsuc F, Brinkmann H, Philippe H (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6:361–375CrossRefPubMedGoogle Scholar
  19. Dobson CM, Wai T, Leclerc D et al (2002) Identification of the gene responsible for the cblA complementation group of vitamin B12-responsive methylmalonic acidemia based on analysis of prokaryotic gene arrangements. Proc Natl Acad Sci USA 99:15554–15559CrossRefPubMedGoogle Scholar
  20. Doerks T, von Mering C, Bork P (2004) Functional clues for hypothetical proteins based on genomic context analysis in prokaryotes. Nucleic Acids Res 32:6321–6326CrossRefPubMedGoogle Scholar
  21. Dorner E, Boll M (2002) Properties of 2-oxoglutarate:ferredoxin oxidoreductase from Thauera aromatica and its role in enzymatic reduction of the aromatic ring. J Bacteriol 184:3975–3983CrossRefPubMedGoogle Scholar
  22. Dutilh BE, He Y, Hekkelman ML, Huynen MA (2008a) Signature, a web server for taxonomic characterization of sequence samples using signature genes. Nucleic Acids Res 36:W470–W474CrossRefPubMedGoogle Scholar
  23. Dutilh BE, Snel B, Ettema TJ, Huynen MA (2008b) Signature genes as a phylogenomic tool. Mol Biol Evol 25:1659–1667CrossRefPubMedGoogle Scholar
  24. Elkins JG, Podar M, Graham DE et al (2008) A korarchaeal genome reveals insights into the evolution of the Archaea. Proc Natl Acad Sci USA 105:8102–8107CrossRefPubMedGoogle Scholar
  25. Fang G, Rocha E, Danchin A (2005) How essential are nonessential genes? Mol Biol Evol 22:2147–2156CrossRefPubMedGoogle Scholar
  26. Fang G, Rocha EP, Danchin A (2008) Persistence drives gene clustering in bacterial genomes. BMC Genomics 9:4CrossRefPubMedGoogle Scholar
  27. Felsenstein J (1996) Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol 266:418–427 (418–427)CrossRefPubMedGoogle Scholar
  28. Fitz-Gibbon ST, Ladner H, Kim UJ, Stetter KO, Simon MI, Miller JH (2002) Genome sequence of the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. Proc Natl Acad Sci USA 99:984–989CrossRefPubMedGoogle Scholar
  29. Fuhrman JA, McCallum K, Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature 356:148–149CrossRefPubMedGoogle Scholar
  30. Gao B, Gupta RS (2007) Phylogenomic analysis of proteins that are distinctive of Archaea and its main subgroups and the origin of methanogenesis. BMC Genomics 8:86CrossRefPubMedGoogle Scholar
  31. Gao B, Parmanathan R, Gupta RS (2006) Signature proteins that are distinctive characteristics of Actinobacteria and their subgroups. Antonie van Leeuwenhoek 90:69–91CrossRefPubMedGoogle Scholar
  32. Gao B, Sugiman-Marangos S, Junop MS, Gupta RS (2009) Structural and phylogenetic analysis of a conserved actinobacteria-specific protein (ASP1; SCO1997) from Streptomyces coelicolor. BMC Struct Biol 9:40CrossRefPubMedGoogle Scholar
  33. Garrett RA, Klenk H-P (eds) (2006) Archaea: evolution, physiology and molecular biology. Blackwell Publishing, OxfordGoogle Scholar
  34. Garrity GM, Holt JG (2001) Phylum AI. Crenarchaeota phy. nov. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology volume 1: the Archaea and the deeply branching and phototrophic Bacteria, 2nd edn. Springer Verlag, New York, p 169Google Scholar
  35. Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238PubMedGoogle Scholar
  36. Graham DE, Overbeek R, Olsen GJ, Woese CR (2000) An archaeal genomic signature. Proc Natl Acad Sci USA 97:3304–3308CrossRefPubMedGoogle Scholar
  37. Gribaldo S, Brochier-Armanet C (2006) The origin and evolution of Archaea: a state of the art. Philos Trans R Soc Lond B Biol Sci 361:1007–1022CrossRefPubMedGoogle Scholar
  38. Gribaldo S, Philippe H (2002) Ancient phylogenetic relationships. Theor Popul Biol 61:391–408CrossRefPubMedGoogle Scholar
  39. Gupta RS (1998) Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62:1435–1491PubMedGoogle Scholar
  40. Gupta RS (2001) The branching order and phylogenetic placement of species from completed bacterial genomes, based on conserved indels found in various proteins. Int Microbiol 4:187–202CrossRefPubMedGoogle Scholar
  41. Gupta RS (2009) Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int J Syst Evol Microbiol 59:2510–2526CrossRefPubMedGoogle Scholar
  42. Gupta RS, Griffiths E (2006) Chlamydiae-specific proteins and indels: novel tools for studies. Trends Microbiol 14:527–535CrossRefPubMedGoogle Scholar
  43. Gupta RS, Mathews DW (2010) Signature proteins for the major clades of cyanobacteria. BMC Evol Biol 10:24CrossRefPubMedGoogle Scholar
  44. Gupta RS, Mok A (2007) Phylogenomics and signature proteins for the alpha Proteobacteria and its main groups. BMC Microbiol 7:106CrossRefPubMedGoogle Scholar
  45. Gupta RS, Aitken K, Falah M, Singh B (1994) Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc Natl Acad Sci USA 91:2895–2899CrossRefPubMedGoogle Scholar
  46. Hallam SJ, Konstantinidis KT, Putnam N et al (2006) Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci USA 103:18296–18301CrossRefPubMedGoogle Scholar
  47. Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13:407–412CrossRefPubMedGoogle Scholar
  48. Hershberger KL, Barns SM, Reysenbach AL, Dawson SC, Pace NR (1996) Wide diversity of Crenarchaeota. Nature 384:420CrossRefPubMedGoogle Scholar
  49. Huber H, Stetter KO (2001a) Order I. Thermoproteales Zillig and Stetter 1982, 267, VP emend. Burgaff, Huber and Stetter 1997b, 659 (Effective Publicatin: Zillig and Stetter in Zillig, Stetter, Schafer, Janekovic, Wunderl, Holz and Palm 1981, 224). In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology volume 1: the Archaea and the deeply branching and phototrophic bacteria, 2nd edn. Springer Verlag, New York, p 170Google Scholar
  50. Huber H, Stetter KO (2001b) Order III. Suflolobales Stetter 189d, 496VP (Effective publication: Stetter 1989c, 2250). In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology volume 1: the Archaea and the deeply branching and phototrophic Bacteria, 2nd edn. Springer Verlag, New York, p 198Google Scholar
  51. Huber H, Hohn MJ, Rachel R, Fuchs T, Wimmer VC, Stetter KO (2002) A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417:63–67CrossRefPubMedGoogle Scholar
  52. Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376PubMedGoogle Scholar
  53. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal x. Trends Biochem Sci 23:403–405CrossRefPubMedGoogle Scholar
  54. Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546CrossRefPubMedGoogle Scholar
  55. Kuo CH, Ochman H (2009) The fate of new bacterial genes. FEMS Microbiol Rev 33:38–43CrossRefPubMedGoogle Scholar
  56. Lake JA, Herbold CW, Rivera MC, Servin JA, Skophammer RG (2007) Rooting the tree of life using nonubiquitous genes. Mol Biol Evol 24:130–136CrossRefPubMedGoogle Scholar
  57. Lebedinsky AV, Chernyh NA, Bonch-Osmolovskaya EA (2007) Phylogenetic systematics of microorganisms inhabiting thermal environments. Biochemistry (Mosc) 72:1299–1312CrossRefGoogle Scholar
  58. Lerat E, Daubin V, Ochman H, Moran NA (2005) Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3:e130CrossRefPubMedGoogle Scholar
  59. Liu L, Komori K, Ishino S et al (2001) The archaeal DNA primase: biochemical characterization of the p41–p46 complex from Pyrococcus furiosus. J Biol Chem 276:45484–45490CrossRefPubMedGoogle Scholar
  60. Ludwig W, Klenk H-P (2005) Overview: a phylogenetic backbone and taxonomic framework for prokaryotic systamatics. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology. Springer-Verlag, Berlin, pp 49–65CrossRefGoogle Scholar
  61. Makarova KS, Koonin EV (2005) Evolutionary and functional genomics of the Archaea. Curr Opin Microbiol 8:586–594CrossRefPubMedGoogle Scholar
  62. Margolin W, Wang R, Kumar M (1996) Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin. J Bacteriol 178:1320–1327PubMedGoogle Scholar
  63. Narra HP, Cordes MH, Ochman H (2008) Structural features and the persistence of acquired proteins. Proteomics 8:4772–4781CrossRefPubMedGoogle Scholar
  64. Nercessian O, Reysenbach AL, Prieur D, Jeanthon C (2003) Archaeal diversity associated with in situ samplers deployed on hydrothermal vents on the East Pacific Rise (13 degrees N). Environ Microbiol 5:492–502CrossRefPubMedGoogle Scholar
  65. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740 (Review, 52 refs)CrossRefPubMedGoogle Scholar
  66. Pace NR (2009) Mapping the tree of life: progress and prospects. Microbiol Mol Biol Rev 73:565–576CrossRefPubMedGoogle Scholar
  67. Palmieri G, Di Palo M, Scaloni A, Orru S, Marino G, Sannia G (1996) Glutamate-1-semialdehyde aminotransferase from Sulfolobus solfataricus. Biochem J 320(Pt 2):541–545PubMedGoogle Scholar
  68. Peck JW, Bowden ET, Burbelo PD (2004) Structure and function of human Vps20 and Snf7 proteins. Biochem J 377:693–700CrossRefPubMedGoogle Scholar
  69. Perevalova AA, Kolganova TV, Birkeland NK, Schleper C, Bonch-Osmolovskaya EA, Lebedinsky AV (2008) Distribution of Crenarchaeota representatives in terrestrial hot springs of Russia and Iceland. Appl Environ Microbiol 74:7620–7628CrossRefPubMedGoogle Scholar
  70. Philippe H, Forterre P (1999) The rooting of the universal tree of life is not reliable. J Mol Evol 49:509–523CrossRefPubMedGoogle Scholar
  71. Prangishvilli D, Zillig W, Gierl A, Biesert L, Holz I (1982) DNA-dependent RNA polymerase of thermoacidophilic archaebacteria. Eur J Biochem 122:471–477CrossRefPubMedGoogle Scholar
  72. Rao NA, Talwar R, Savithri HS (2000) Molecular organization, catalytic mechanism and function of serine hydroxymethyltransferase–a potential target for cancer chemotherapy. Int J Biochem Cell Biol 32:405–416CrossRefPubMedGoogle Scholar
  73. Ravin NV, Mardanov AV, Beletsky AV et al (2009) Complete genome sequence of the anaerobic, protein-degrading hyperthermophilic crenarchaeon Desulfurococcus kamchatkensis. J Bacteriol 191:2371–2379CrossRefPubMedGoogle Scholar
  74. Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64:167–174CrossRefPubMedGoogle Scholar
  75. Reigstad LJ, Jorgensen SL, Schleper C (2010) Diversity and abundance of Korarchaeota in terrestrial hot springs of Iceland and Kamchatka. ISME J 4:346–356CrossRefPubMedGoogle Scholar
  76. Reysenbach A-L (2001) Class I. thermoprotei class. nov. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology volume 1: the Archaea and the deeply branching and phototrophic Bacteria, 2nd edn. Springer Verlag, New York, p 169Google Scholar
  77. Reysenbach AL, Ehringer M, Hershberger K (2000) Microbial diversity at 83 degrees C in Calcite Springs, Yellowstone National Park: another environment where the Aquificales and “Korarchaeota” coexist. Extremophiles 4:61–67PubMedGoogle Scholar
  78. Reysenbach AL, Liu Y, Banta AB et al (2006) A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442:444–447CrossRefPubMedGoogle Scholar
  79. Rivera MC, Lake JA (1992) Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257:74–76CrossRefPubMedGoogle Scholar
  80. Rokas A, Holland PW (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459CrossRefPubMedGoogle Scholar
  81. Schauss K, Focks A, Leininger S et al (2009) Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 11:446–456CrossRefPubMedGoogle Scholar
  82. Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3:479–488CrossRefPubMedGoogle Scholar
  83. Siew N, Fischer D (2003) Analysis of singleton ORFans in fully sequenced microbial genomes. Proteins 53:241–251CrossRefPubMedGoogle Scholar
  84. Singh B, Gupta RS (2009) Conserved inserts in the Hsp60 (GroEL) and Hsp70 (DnaK) proteins are essential for cellular growth. Mol Genet Genomics 281:361–373CrossRefPubMedGoogle Scholar
  85. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, Miller NE (2001) Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res 29:1097–1106CrossRefPubMedGoogle Scholar
  86. Stackebrandt E (2006) Defining taxonomic ranks. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 29–57CrossRefGoogle Scholar
  87. Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285–1297PubMedGoogle Scholar
  88. Uemori T, Sato Y, Kato I, Doi H, Ishino Y (1997) A novel DNA polymerase in the hyperthermophilic archaeon, Pyrococcus furiosus: gene cloning, expression, and characterization. Genes Cells 2:499–512CrossRefPubMedGoogle Scholar
  89. Walsh DA, Doolittle WF (2005) The real ‘domains’ of life. Curr Biol 15:R237–R240CrossRefPubMedGoogle Scholar
  90. Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090CrossRefPubMedGoogle Scholar
  91. Woese CR, Gupta R, Hahn CM, Zillig W, Tu J (1984) The phylogenetic relationships of three sulfur dependent archaebacteria. Syst Appl Microbiol 5:97–105PubMedGoogle Scholar
  92. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579CrossRefPubMedGoogle Scholar
  93. Xu Z, Hao B (2009) CVTree update: a newly designed phylogenetic study platform using composition vectors and whole genomes. Nucleic Acids Res 37:W174–W178CrossRefPubMedGoogle Scholar
  94. Yang Z (2005) The power of phylogenetic comparison in revealing protein function. Proc Natl Acad Sci USA 102:3179–3180CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Biochemistry and Biomedical SciencesMcMaster UniversityHamiltonCanada

Personalised recommendations