Antonie van Leeuwenhoek

, Volume 90, Issue 1, pp 69–91 | Cite as

Signature proteins that are distinctive characteristics of Actinobacteria and their subgroups

Article

Abstract

The Actinobacteria constitute one of the main phyla of Bacteria. Presently, no morphological and very few molecular characteristics are known which can distinguish species of this highly diverse group. In this work, we have analyzed the genomes of four actinobacteria (viz. Mycobacterium leprae TN, Leifsonia xyli subsp. xyli str. CTCB07, Bifidobacterium longum NCC2705 and Thermobifida fusca YX) to search for proteins that are unique to Actinobacteria. Our analyses have identified 233 actinobacteria-specific proteins, homologues of which are generally not present in any other bacteria. These proteins can be grouped as follows: (i) 29 proteins uniquely present in most sequenced actinobacterial genomes; (ii) 6 proteins present in almost all actinobacteria except Bifidobacterium longum and another 37 proteins absent in B. longum and few other species; (iii) 11 proteins which are mainly present in Corynebacterium, Mycobacterium and Nocardia (CMN) subgroup as well as Streptomyces, T. fusca and Frankia sp., but they are not found in Bifidobacterium and Micrococcineae; (iv) 8 proteins that are specific for T. fusca and Streptomyces species, plus 2 proteins also present in the Frankia species; (v) 13 proteins that are specific for the Corynebacterineae or the CMN group; (vi) 14 proteins only found in Mycobacterium and Nocardia; (vii) 24 proteins unique to different Mycobacterium species; (viii) 8 proteins specific to the Micrococcineae; (ix) 85 proteins which are distributed sporadically in actinobacterial species. Additionally, many examples of lateral gene transfer from Actinobacteria to Magnetospirillum magnetotacticum have also been identified. The identified proteins provide novel molecular means for defining and circumscribing the Actinobacteria phylum and a number of subgroups within it. The distribution of these proteins also provides useful information regarding interrelationships among the actinobacterial subgroups. Most of these proteins are of unknown function and studies aimed at understanding their cellular functions should reveal common biochemical and physiological characteristics unique to either all actinobacteria or particular subgroups of them. The identified proteins also provide potential targets for development of drugs that are specific for actinobacteria.

Keywords

Actinobacteria Actinobacterial taxonomy Bacterial phylogeny Branching order CMN bacteria Group-specific proteins Magnetospirillum Mycobacteria 

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References

  1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J.H., Zhang Z., Miller W., Lipman D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402PubMedCrossRefGoogle Scholar
  2. Balows A., Trüper H.G., Dworkin M., Harder W., Schleifer K.H. 1992. The Prokaryotes. Springer-Verlag, New YorkGoogle Scholar
  3. Bazylinski D.A., Frankel R.B. 2004. Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2:217–230PubMedCrossRefGoogle Scholar
  4. Belanger A.E., Besra G.S., Ford M.E., Mikusova K., Belisle J.T., Brennan P.J., Inamine J.M. 1996. The embAB genes of Mycobacterium avium encode an arabinosyl transferase involved in cell wall arabinan biosynthesis that is the target for the antimycobacterial drug ethambutol. Proc Natl Acad Sci USA. 93:11919–11924PubMedCrossRefGoogle Scholar
  5. Benson D.R., Silvester W.B., (1993). Biology of Frankia Strains, Actinomycete Symbionts of Actinorhizal Plants. Microbiol Rev. 57:293–319PubMedGoogle Scholar
  6. Bentley S.D., Brosch R., Gordon S.V., Hopwood D.A., Cole S.T., (2004). Genomics of Actinobacteria, the high G+C Gram-positive bacteria. In: Fraser C.M., Read T.D., Nelson K.E., (eds) Microbial Genomes. Humana Press, Totowa, NJ, pp. 333–359Google Scholar
  7. Bentley S.D., Chater K.F., Cerdeno-Tarraga A.M., Challis G.L., Thomson N.R., James K.D., Harris D.E., Quail M.A., Kieser H., Harper D., Bateman A., Brown S., Chandra G., Chen C.W., Collins M., Cronin A., Fraser A., Goble A., Hidalgo J., Hornsby T., Howarth S., Huang C.H., Kieser T., Larke L., Murphy L., Oliver K., O’Neil S., Rabbinowitsch E., Rajandream M.A., Rutherford K., Rutter S., Seeger K., Saunders D., Sharp S., Squares R., Squares S., Taylor K., Warren T., Wietzorrek A., Woodward J., Barrell B.G., Parkhill J., Hopwood D.A., (2002). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147PubMedCrossRefGoogle Scholar
  8. Bentley S.D., Maiwald M., Murphy L.D., Pallen M.J., Yeats C.A., Dover L.G., Norbertczak H.T., Besra G.S., Quail M.A., Harris D.E., von Herbay A., Goble A., Rutter S., Squares R., Squares S., Barrell B.G., Parkhill J., Relman D.A., (2003). Sequencing and analysis of the genome of the Whipple’s disease bacterium Tropheryma whipplei. Lancet 361:637–644PubMedCrossRefGoogle Scholar
  9. Bentley S.D., Parkhill J., (2004). Comparative genomic structure of prokaryotes. Annu. Rev. Genet. 38:771–792PubMedCrossRefGoogle Scholar
  10. Berg S., Starbuck J., Torrelles J.B., Vissa V.D., Crick D.C., Chatterjee D., Brennan P.J., (2005). Roles of conserved proline and glycosyltransferase motifs of embC in biosynthesis of lipoarabinomannan. J. Biol. Chem. 280:5651–5663PubMedCrossRefGoogle Scholar
  11. Boone D.R. 2001. Bergey’s Manual of systematic bacteriology, SpringerGoogle Scholar
  12. Brennan P.J. (2003). Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83:91–97PubMedCrossRefGoogle Scholar
  13. Brennan P.J., Nikaido H., (1995). The envelope of mycobacteria. Annu. Rev. Biochem. 64:29–63PubMedCrossRefGoogle Scholar
  14. Bruggemann H., Henne A., Hoster F., Liesegang H., Wiezer A., Strittmatter A., Hujer S., Durre P., Gottschalk G., (2004). The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305:671–673PubMedCrossRefGoogle Scholar
  15. Cerdeno-Tarraga A.M., Efstratiou A., Dover L.G., Holden M.T.G., Pallen M., Bentley S.D., Besra G.S., Churcher C., James K.D., De Zoysa A., Chillingworth T., Cronin A., Dowd L., Feltwell T., Hamlin N., Holroyd S., Jagels K., Moule S., Quail M.A., Rabbinowitsch E., Rutherford K.M., Thomson N.R., Unwin L., Whitehead S., Barrell B.G., Parkhill J., (2003). The complete genome sequence and analysis of Corynebacterium diphtheriae NCTC13129. Nucleic Acids Res. 31:6516–6523PubMedCrossRefGoogle Scholar
  16. Coenye T., Gevers D., de Peer Y.V., Vandamme P., Swings J., (2005). Towards a prokaryotic genomic taxonomy. FEMS Microbiol. Rev. 29:147–167PubMedCrossRefGoogle Scholar
  17. Cole S.T. (2002). Comparative and functional genomics of the Mycobacterium tuberculosis complex. Microbiology 148:2919–2928PubMedGoogle Scholar
  18. Cole S.T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., Gordon S.V., Eiglmeier K., Gas S., Barry C.E., Tekaia F., Badcock K., Basham D., Brown D., Chillingworth T., Conner R., Davies R., Devlin K., Feltwell T., Gentles S., Hamlin N., Holroyd S., Hornsby T., Jagels K., Krogh A., McLean J., Moule S., Murphy L., Oliver K., Osborne J., Quail M.A., Rajandream M.A., Rogers J., Rutter S., Seeger K., Skelton J., Squares R., Squares S., Sulston J.E., Taylor K., Whitehead S., Barrell B.G., (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence (vol 393, pg 537, 1998). Nature 396:190–198CrossRefGoogle Scholar
  19. Cole S.T., Eiglmeier K., Parkhill J., James K.D., Thomson N.R., Wheeler P.R., Honore N., Garnier T., Churcher C., Harris D., Mungall K., Basham D., Brown D., Chillingworth T., Connor R., Davies R.M., Devlin K., Duthoy S., Feltwell T., Fraser A., Hamlin N., Holroyd S., Hornsby T., Jagels K., Lacroix C., Maclean J., Moule S., Murphy L., Oliver K., Quail M.A., Rajandream M.A., Rutherford K.M., Rutter S., Seeger K., Simon S., Simmonds M., Skelton J., Squares R., Squares S., Stevens K., Taylor K., Whitehead S., Woodward J.R., Barrell B.G., (2001). Massive gene decay in the leprosy bacillus. Nature 409:1007–1011PubMedCrossRefGoogle Scholar
  20. Collier L., Balows A., Sussman M., (1998). Topley &Wilson’s Microbiology and Microbial Infections, Vol. 2, Systematic Bacteriology. Arnold, LondonGoogle Scholar
  21. Daffe M., Draper P., (1998). The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39:131–203PubMedCrossRefGoogle Scholar
  22. Daubin V., Ochman H., (2004). Bacterial genomes as new gene homes: the genealogy of ORFans in E. coli. Genome Res. 14:1036–1042PubMedCrossRefGoogle Scholar
  23. Domenech P., Barry C.E., Cole S.T., (2001). Mycobacterium tuberculosis in the post-genomic age. Curr. Opin. Microbiol. 4:28–34PubMedCrossRefGoogle Scholar
  24. Embley T.M., Stackebrandt E., (1994). The molecular phylogeny and systematics of the actinomycetes. Annu. Rev. Microbiol. 48:257–289PubMedGoogle Scholar
  25. Fleischmann R.D., Alland D., Eisen J.A., Carpenter L., White O., Peterson J., Deboy R., Dodson R., Gwinn M., Haft D., Hickey E., Kolonay J.F., Nelson W.C., Umayam L.A., Ermolaeva M., Salzberg S.L., Delcher A., Utterback T., Weidman J., Khouri H., Gill J., Mikula A., Bishai W., Jacobs W.R., Venter J.C., Fraser C.M., (2002). Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. J. Bacteriol. 184:5479–5490PubMedCrossRefGoogle Scholar
  26. Fraser C.M., Read T.D., Nelson K.E. (eds). (2004). Microbial Genomes. Humana Press, Totowa, NJGoogle Scholar
  27. Gao B., Gupta R.S., (2005). Conserved indels in protein sequences that are characteristic of the phylum Actinobacteria. Int. J. Syst. Evol. Microbiol. 151:2647–2657Google Scholar
  28. Garnier T., Eiglmeier K., Camus J.C., Medina N., Mansoor H., Pryor M., Duthoy S., Grondin S., Lacroix C., Monsempe C., Simon S., Harris B., Atkin R., Doggett J., Mayes R., Keating L., Wheeler P.R., Parkhill J., Barrell B.G., Cole S.T., Gordon S.V., Hewinson R.G., (2003). The complete genome sequence of Mycobacterium bovis. Proc. Natl. Acad. Sci. USA 100:7877–7882PubMedCrossRefGoogle Scholar
  29. Garrity G.M., Holt J.G., (2001). The road map to the manual. In: Boone D.R., Castenholz R.W. (eds) Bergey’s Manual of Systematic Bacteriology. Springer-Verlag, Berlin, pp. 119–166Google Scholar
  30. Gogarten J.P., Townsend J.P., (2005). Horizontal gene transfer, genome innovation and evolution. Nat. Rev. Microbiol. 3:679–687PubMedCrossRefGoogle Scholar
  31. Goodfellow M., Williams S.T., (1983). Ecology of Actinomycetes. Annu. Rev. Microbiol. 37:189–216PubMedCrossRefGoogle Scholar
  32. Gordon S.V., Eiglmeier K., Garnier T., Brosch R., Parkhill J., Barrell B., Cole S.T., Hewinson R.G., (2001). Genomics of Mycobacterium bovis. Tuberculosis 81:157–163PubMedCrossRefGoogle Scholar
  33. Griffiths E., Gupta R.S., (2004). Signature sequences in diverse proteins provide evidence for the late divergence of the order Aquificales. Intl Microbiol. 7:41–52Google Scholar
  34. Griffiths E., Petrich A., Gupta R.S., (2005). Conserved indels in essential proteins that are distinctive characteristics of Chlamydiales and provide novel means for their identification. Microbiology 151:2647–2657PubMedCrossRefGoogle Scholar
  35. Griffiths E., Ventresca M.S., Gupta R.S. 2006. BLAST screening of chlamydial genomes to identify signature proteins that are unique for the Chlamydiales, Chlamydiaceae, Chlamydophila and Chlamydia groups of species. BMC Genomics 7:14Google Scholar
  36. Gupta R.S. (1998). Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol. Mol. Biol. Rev. 62:1435–1491PubMedGoogle Scholar
  37. Gupta R.S. (2000). The phylogeny of Proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol. Rev. 24:367–402PubMedCrossRefGoogle Scholar
  38. Gupta R.S. (2004). The Phylogeny and Signature Sequences characteristics of Fibrobacters, Chlorobi and Bacteroidetes. Crit. Rev. Microbiol. 30:123–143PubMedCrossRefGoogle Scholar
  39. Gupta R.S. (2005). Protein signatures distinctive of Alpha proteobacteria and its subgroups and a model for Alpha proteobacterial evolution. Crit. Rev. Microbiol. 31:135CrossRefGoogle Scholar
  40. Ikeda H., Ishikawa J., Hanamoto A., Shinose M., Kikuchi H., Shiba T., Sakaki Y., Hattori M., Omura S., (2003). Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 21:526–531PubMedCrossRefGoogle Scholar
  41. Ishikawa J., Yamashita A., Mikami Y., Hoshino Y., Kurita H., Hotta K., Shiba T., Hattori M., (2004). The complete genomic sequence of Nocardia farcinica IFM 10152. Proc. Natl. Acad. Sci. USA 101:14925–14930PubMedCrossRefGoogle Scholar
  42. Kainth P., Gupta R.S., (2005). Signature proteins that are distinctive of alpha proteobacteria. BMC Genomics 6:94PubMedCrossRefGoogle Scholar
  43. Kalinowski J., Bathe B., Bartels D., Bischoff N., Bott M., Burkovski A., Dusch N., Eggeling L., Eikmanns B.J., Gaigalat L., Goesmann A., Hartmann M., Huthmacher K., Kramer R., Linke B., McHardy A.C., Meyer F., Mockel B., Pfefferle W., Puhler A., Rey D.A., Ruckert C., Rupp O., Sahm H., Wendisch V.F., Wiegrabe I., Tauch A., (2003). The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J. Biotechnol. 104:5–25PubMedCrossRefGoogle Scholar
  44. Karlin S., Altschul S.F., (1990). Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc. Natl. Acad. Sci. USA 87:2264–2268PubMedCrossRefGoogle Scholar
  45. Karlin S., Campbell A.M., Mrázek J. (1998). Comparative DNA analysis across diverse genomes. Annu. Rev. Genet. 32:185–225PubMedCrossRefGoogle Scholar
  46. Lechevalier H.A., Lechevalier M.P., (1967). Biology of Actinomycetes. Annu. Rev. Microbiol. 21:71–100PubMedCrossRefGoogle Scholar
  47. Lerat E., Daubin V., Moran N.A., (2003). From gene trees to organismal phylogeny in prokaryotes: the case of the gamma-proteobacteria. PLoS. Biol. 1:E19PubMedCrossRefGoogle Scholar
  48. Ludwig W., Klenk H.-P., (2001). Overview: A phylogenetic backbone and taxonomic framework for prokaryotic systamatics. In: Boone D.R., Castenholz R.W., (eds) Bergey’s Manual of Systematic Bacteriology. Springer-Verlag, Berlin, pp. 49–65Google Scholar
  49. Mazumder R., Natale D.A., Murthy S., Thiagarajan R., Wu C.H., (2005). Computational identification of strain-, species- and genus-specific proteins. BMC Bioinform. 6:279CrossRefGoogle Scholar
  50. McAlpine J.B., Bachmann B.O., Piraee M., Tremblay S., Alarco A.M., Zazopoulos E., Farnet C.M., (2005). Microbial Genomics as a guide to drug discovery and structural elucidation: ECO-02301, a novel antifungal agent, as an example. J. Nat. Prod. 68:493–496PubMedCrossRefGoogle Scholar
  51. Monteiro-Vitorello C.B., Camargo L.E.A., Van Sluys M.A., Kitajima J.P., Truffi D., do Amaral A.M., Harakava R., de Oliveira J.C.F., Wood D., de Oliveira M.C., Miyaki C., Takita M.A., da Silva A.C.R., Furlan L.R., Carraro D.M., Camarotte G., Almeida N.F., Carrer H., Coutinho L.L., El Dorry H.A., Ferro M.I.T., Gagliardi P.R., Giglioti E., Goldman M.H.S., Goldman G.H., Kimura E.T., Ferro E.S., Kuramae E.E., Lemos E.G.M., Lemos M.V.F., Mauro S.M.Z., Machado M.A., Marino C.L., Menck C.F., Nunes L.R., Oliveira R.C., Pereira G.G., Siqueira W., de Souza A.A., Tsai S.M., Zanca A.S., Simpson A.J.G., Brumbley S.M., Setubal J.C., (2004). The genome sequence of the gram-positive sugarcane pathogen Leifsonia xyli subsp xyli. Mol. Plant Microb. Interact. 17:827–836CrossRefGoogle Scholar
  52. Moran N.A., Wernegreen J.J., (2000). Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15:321–326PubMedCrossRefGoogle Scholar
  53. Morse R., O’Hanlon K., Collins M.D., (2002). Phylogenetic, amino acid content and indel analyses of the beta subunit of DNA-dependent RNA polymerase of gram-positive and gram-negative bacteria. Int. J. Syst. Evol. Microbiol. 52:1477–1484PubMedCrossRefGoogle Scholar
  54. Nishio Y., Nakamura Y., Kawarabayasi Y., Usuda Y., Kimura E., Sugimoto S., Matsui K., Yamagishi A., Kikuchi H., Ikeo K., Gojobori T., (2003). Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res. 13:1572–1579PubMedCrossRefGoogle Scholar
  55. Pedulla M.L., Ford M.E., Houtz J.M., Karthikeyan T., Wadsworth C., Lewis J.A., Jacobs-Sera D., Falbo J., Gross J., Pannunzio N.R., Brucker W., Kumar V., Kandasamy J., Keenan L., Bardarov S., Kriakov J., Lawrence J.G., Jacobs W.R., Hendrix R.W., Hatfull G.F., (2003). Origins of highly mosaic mycobacteriophage genomes. Cell 113:171–182PubMedCrossRefGoogle Scholar
  56. Puech V., Chami M., Lemassu A., Laneelle M.A., Schiffler B., Gounon P., Bayan N., Benz R., Daffe M., (2001). Structure of the cell envelope of corynebacteria: importance of the non-covalently bound lipids in the formation of the cell wall permeability barrier and fracture plane. Microbiology 147:1365–1382PubMedGoogle Scholar
  57. Raoult D., Ogata H., Audic S., Robert C., Suhre K., Drancourt M., Claverie J.M., (2003). Tropheryma whipplei twist: a human pathogenic Actinobacteria with a reduced genome. Genome Res. 13:1800–1809PubMedGoogle Scholar
  58. Ravel J., DiRuggiero J., Robb F.T., Hill R.T., (2000). Cloning and sequence analysis of the mercury resistance operon of Streptomyces sp. strain CHR28 reveals a novel putative second regulatory gene. J. Bacteriol. 182:2345–2349PubMedCrossRefGoogle Scholar
  59. Roller C., Ludwig W., Schleifer K.H. (1992). Gram-positive bacteria with a high DNA G+C content are characterized by a common insertion within their 23S rRNA genes. J. Gen. Microbiol. 138:167–175Google Scholar
  60. Rother D., Mattes R., Altenbuchner J., (1999). Purification and characterization of MerR, the regulator of the broad-spectrum mercury resistance genes in Streptomyces lividans 1326. Mol. Gen. Genet. 262:154–162PubMedCrossRefGoogle Scholar
  61. Schell M.A., Karmirantzou M., Snel B., Vilanova D., Berger B., Pessi G., Zwahlen M.C., Desiere F., Bork P., Delley M., Pridmore R.D., Arigoni F., (2002). The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. USA 99:14422–14427PubMedCrossRefGoogle Scholar
  62. Schorey J.S., Li Q.L., Mccourt D.W., Bongmastek M., Clarkcurtiss J.E., Ratliff T.L., Brown E.J., (1995). A mycobacterium-leprae gene encoding a fibronectin-binding protein is used for efficient invasion of epithelial-cells and schwann-cells. Infect. Immun. 63:2652–2657PubMedGoogle Scholar
  63. Soliveri J.A., Gomez J., Bishai W.R., Chater K.F., (2000). Multiple paralogous genes related to the Streptomyces coelicolor developmental regulatory gene whiB are present in Streptomyces and other actinomycetes. Microbiol.-Uk 146:333–343Google Scholar
  64. Stackebrandt E., Rainey F.A., WardRainey N.L., (1997). Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int. J. Syst. Bacteriol. 47:479–491CrossRefGoogle Scholar
  65. Stackebrandt E., Schumann P., (2000). Introduction to the taxonomy of actinobacteria. In: Dworkin M., et al. (eds) The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community. Springer-Verlag, New York, http://www.141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=291
  66. Sutcliffe I.C. (1998). Cell envelope composition and organisation in the genus Rhodococcus. Antonie van Leeuwenhoek 74: 49–58PubMedCrossRefGoogle Scholar
  67. Sutcliffe I.C., Harrington D.J., (2004). Lipoproteins of Mycobacterium tuberculosis: an abundant and functionally diverse class of cell envelope components. FEMS Microbiol. Rev. 28:645–659PubMedCrossRefGoogle Scholar
  68. Sutcliffe I.C., Russell R.R., (1995). Lipoproteins of gram-positive bacteria. J. Bacteriol. 177:1123–1128PubMedGoogle Scholar
  69. Tauch A., Kaiser O., Hain T., Goesmann A., Weisshaar B., Albersmeier A., Bekel T., Bischoff N., Brune I., Chakraborty T., Kalinowski J., Meyer F., Rupp O., Schneiker S., Viehoever P., Puhler A., (2005). Complete genome sequence and analysis of the multiresistant nosocomial pathogen Corynebacterium jeikeium K411, a lipid-requiring bacterium of the human skin flora. J. Bacteriol. 187:4671–4682PubMedCrossRefGoogle Scholar
  70. Ueda K., Ohno M., Yamamoto K., Nara H., Mori Y., Shimada M., Hayashi M., Oida H., Terashima Y., Nagata M., Beppu T., (2001). Distribution and diversity of symbiotic thermophiles, Symbiobacterium thermophilum and related bacteria, in natural environments. Appl. Environ. Microbiol. 67:3779–3784PubMedCrossRefGoogle Scholar
  71. Ueda K., Yamashita A., Ishikawa J., Shimada M., Watsuji T., Morimura K., Ikeda H., Hattori M., Beppu T., (2004). Genome sequence of Symbiobacterium thermophilum, an uncultivable bacterium that depends on microbial commensalism. Nucleic Acids Res. 32:4937–4944PubMedCrossRefGoogle Scholar
  72. Yang Z. (2005). The power of phylogenetic comparison in revealing protein function. Proc. Natl. Acad. Sci. USA 102:3179–3180PubMedCrossRefGoogle Scholar
  73. Zazopoulos E., Huang K.X., Staffa A., Liu W., Bachmann B.O., Nonaka K., Ahlert J., Thorson J.S., Shen B., Farnet C.M., (2003). A genomics-guided approach for discovering and expressing cryptic metabolic pathways. Nat. Biotechnol. 21:187–190PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Department of Biochemistry and Biomedical ScienceMcMaster UniversityHamiltonCanada

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