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Archaea
Volume 2010, Article ID 426239, 11 pages
http://dx.doi.org/10.1155/2010/426239
Research Article

Towards a Systems Approach in the Genetic Analysis of Archaea: Accelerating Mutant Construction and Phenotypic Analysis in Haloferax volcanii

Department of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611-0700, USA

Received 2 September 2010; Accepted 24 October 2010

Academic Editor: Li Huang

Copyright © 2010 Ian K. Blaby et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. R. Woese and G. E. Fox, “Phylogenetic structure of the prokaryotic domain: the primary kingdoms,” Proceedings of the National Academy of Sciences of the United States of America, vol. 74, no. 11, pp. 5088–5090, 1977. View at Google Scholar · View at Scopus
  2. S.-V. Albers, N.-K. Birkeland, A. J. M. Driessen et al., “SulfoSYS (Sulfolobus Systems Biology): towards a silicon cell model for the central carbohydrate metabolism of the archaeon Sulfolobus solfataricus under temperature variation,” Biochemical Society Transactions, vol. 37, no. 1, pp. 58–64, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. T. K. Pham, P. Sierocinski, J. Van Der Oost, and P. C. Wright, “Quantitative proteomic analysis of Sulfolobus solfataricus membrane proteins,” Journal of Proteome Research, vol. 9, no. 2, pp. 1165–1172, 2010. View at Publisher · View at Google Scholar
  4. S. Berkner and G. Lipps, “Genetic tools for Sulfolobus spp.: vectors and first applications,” Archives of Microbiology, vol. 190, no. 3, pp. 217–230, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Wagner, S. Berkner, M. Ajon, A. J. M. Driessen, G. Lipps, and S.-V. Albers, “Expanding and understanding the genetic toolbox of the hyperthermophilic genus Sulfolobus,” Biochemical Society Transactions, vol. 37, no. 1, pp. 97–101, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Sato, T. Fukui, H. Atomi, and T. Imanaka, “Improved and versatile transformation system allowing multiple genetic manipulations of the hyperthermophilic archaeon Thermococcus kodakaraensis,” Applied and Environmental Microbiology, vol. 71, no. 7, pp. 3889–3899, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Sato, T. Fukui, H. Atomi, and T. Imanaka, “Targeted gene disruption by homologous recombination in the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1,” Journal of Bacteriology, vol. 185, no. 1, pp. 210–220, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. I. Waege, G. Schmid, S. Thumann, M. Thomm, and W. Hausner, “Shuttle vector-based transformation system for pyrococcus furiosus,” Applied and Environmental Microbiology, vol. 76, no. 10, pp. 3308–3313, 2010. View at Publisher · View at Google Scholar
  9. C. J. Bult, O. White, G. J. Olsen et al., “Complete genome sequence of the Methanogenic archaeon, Methanococcus jannaschii,” Science, vol. 273, no. 5278, pp. 1058–1073, 1996. View at Google Scholar · View at Scopus
  10. B. C. Moore and J. A. Leigh, “Markerless mutagenesis in Methanococcus maripaludis demonstrates roles for alanine dehydrogenase, alanine racemase, and alanine permease,” Journal of Bacteriology, vol. 187, no. 3, pp. 972–979, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. M. A. Pritchett, J. K. Zhang, and W. W. Metcalf, “Development of a markerless genetic exchange method for Methanosarcina acetivorans C2A and its use in construction of new genetic tools for methanogenic archaea,” Applied and Environmental Microbiology, vol. 70, no. 3, pp. 1425–1433, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Dyall-Smith, The Halohandbook: Protocols for Halobacterial Genetics, vol. 6.01, 2006, http://www.microbiol.unimelb.edu.au/micro/staff/mds/HaloHandbook/.
  13. A. Zaigler, S. C. Schuster, and J. Soppa, “Construction and usage of a onefold-coverage shotgun dna microarray to characterize the metabolism of the archaeon Haloferax volcanii,” Molecular Microbiology, vol. 48, no. 4, pp. 1089–1105, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Hartman, C. Norais, J. Badger et al., “The complete genome sequence of Haloferax volcanii DS2, a model archaeon,” PLoS One, vol. 5, article no. e9605, 2010. View at Google Scholar
  15. T. Allers, S. Barak, S. Liddell, K. Wardell, and M. Mevarech, “Improved strains and plasmid vectors for conditional overexpression of His-tagged proteins in Haloferax volcanii,” Applied and Environmental Microbiology, vol. 76, no. 6, pp. 1759–1769, 2010. View at Publisher · View at Google Scholar
  16. T. Allers, H.-P. Ngo, M. Mevarech, and R. G. Lloyd, “Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes,” Applied and Environmental Microbiology, vol. 70, no. 2, pp. 943–953, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. B. El Yacoubi, G. Phillips, I. K. Blaby et al., “A gateway platform for functional genomics in Haloferax volcanii: deletion of three tRNA modification genes,” Archaea, vol. 2, no. 4, pp. 211–219, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Bisle, A. Schmidt, B. Scheibe et al., “Quantitative profiling of the membrane proteome in Halophilic archaeon,” Molecular and Cellular Proteomics, vol. 5, no. 9, pp. 1543–1558, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Lange, A. Zaigler, M. Hammelmann et al., “Genome-wide analysis of growth phase-dependent translational and transcriptional regulation in halophilic archaea,” BMC Genomics, vol. 8, article no. 415, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Tebbe, A. Schmidt, K. Konstantinidis et al., “Life-style changes of a halophilic archaeon analyzed by quantitative proteomics,” Proteomics, vol. 9, no. 15, pp. 3843–3855, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Twellmeyer, A. Wende, J. Wolfertz et al., “Microarray analysis in the archaeon Halobacterium salinarum strain R1,” PLoS ONE, vol. 2, no. 10, article no. e1064, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Y. Gerdes, M. D. Scholle, J. W. Campbell et al., “Experimental determination and system level analysis of essential genes in Escherichia coli MG1655,” Journal of Bacteriology, vol. 185, no. 19, pp. 5673–5684, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. N. Suzuki, N. Okai, H. Nonaka, Y. Tsuge, M. Inui, and H. Yukawa, “High-throughput transposon mutagenesis of Corynebacterium glutamicum and construction of a single-gene disruptant mutant library,” Applied and Environmental Microbiology, vol. 72, no. 5, pp. 3750–3755, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. B. J. Akerley, E. J. Rubin, V. L. Novick, K. Amaya, N. Judson, and J. J. Mekalanos, “A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 2, pp. 966–971, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. M. A. Jacobs, A. Alwood, I. Thaipisuttikul et al., “Comprehensive transposon mutant library of Pseudomonas aeruginosa,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 14339–14344, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. N. T. Liberati, J. M. Urbach, S. Miyata et al., “An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 8, pp. 2833–2838, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Baba, T. Ara, M. Hasegawa et al., “Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection,” Molecular Systems Biology, vol. 2, article no. 2006.0008, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Giaever, A. M. Chu, L. Ni et al., “Functional profiling of the Saccharomyces cerevisiae genome,” Nature, vol. 418, no. 6896, pp. 387–391, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Kobayashi, S. D. Ehrlich, A. Albertini et al., “Essential Bacillus subtilis genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 8, pp. 4678–4683, 2003. View at Publisher · View at Google Scholar
  30. M. E. Hillenmeyer, E. Ericson, R. W. Davis, C. Nislow, D. Koller, and G. Giaever, “Systematic analysis of genome-wide fitness data in yeast reveals novel gene function and drug action,” Genome Biology, vol. 11, no. 3, article no. r30, 2010. View at Publisher · View at Google Scholar
  31. M. E. Hillenmeyer, E. Fung, J. Wildenhain et al., “The chemical genomic portrait of yeast: uncovering a phenotype for all genes,” Science, vol. 320, no. 5874, pp. 362–365, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Tamae, A. Liu, K. Kim et al., “Determination of antibiotic hypersensitivity among 4,000 single-gene-knockout mutants of Escherichia coli,” Journal of Bacteriology, vol. 190, no. 17, pp. 5981–5988, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. S. J. Kaczowka and J. A. Maupin-Furlow, “Subunit topology of two 20S proteasomes from Haloferax volcanii,” Journal of Bacteriology, vol. 185, no. 1, pp. 165–174, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. V. de Crécy-Lagard, C. Brochier-Armanet, J. Urbonaviius et al., “Biosynthesis of wyosine derivatives in tRNA: an ancient and highly diverse pathway in archaea,” Molecular Biology and Evolution, vol. 27, no. 9, pp. 2062–2077, 2010. View at Publisher · View at Google Scholar
  35. B. Zhu, G. Cai, E. O. Hall, and G. J. Freeman, “In-Fusion assembly: seamless engineering of multidomain fusion proteins, modular vectors, and mutations,” BioTechniques, vol. 43, no. 3, pp. 354–359, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Auxilien, F. El Khadali, A. Rasmussen, S. Douthwaite, and H. Grosjean, “Archease from Pyrococcus abyssi improves substrate specificity and solubility of a tRNA m5C methyltransferase,” Journal of Biological Chemistry, vol. 282, no. 26, pp. 18711–18721, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Gupta, “Halobacterium volcanii tRNAs. Identification of 41 tRNAs covering all amino acids, and the sequences of 33 class I tRNAs,” Journal of Biological Chemistry, vol. 259, no. 15, pp. 9461–9471, 1984. View at Google Scholar · View at Scopus
  38. R. M. McCarty, Á. Somogyi, G. Lin, N. E. Jacobsen, and V. Bandarian, “The deazapurine biosynthetic pathway revealed: in vitro enzymatic synthesis of PreQ0 from guanosine 5-triphosphate in four steps,” Biochemistry, vol. 48, no. 18, pp. 3847–3852, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. J. S. Reader, D. Metzgar, P. Schimmel, and V. De Crécy-Lagard, “Identification of four genes necessary for biosynthesis of the modified nucleoside queuosine,” Journal of Biological Chemistry, vol. 279, no. 8, pp. 6280–6285, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Watanabe, M. Matsuo, S. Tanaka et al., “Biosynthesis of archaeosine, a novel derivative of 7-deazaguanosine specific to archaeal tRNA, proceeds via a pathway involving base replacement on the tRNA polynucleotide chain,” Journal of Biological Chemistry, vol. 272, no. 32, pp. 20146–20151, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Sprinzl, C. Steegborn, F. Hübel, and S. Steinberg, “Compilation of tRNA sequences and sequences of tRNA genes,” Nucleic Acids Research, vol. 24, no. 1, pp. 68–72, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Altman-Price and M. Mevarech, “Genetic evidence for the importance of protein acetylation and protein deacetylation in the halophilic archaeon Haloferax volcanii,” Journal of Bacteriology, vol. 191, no. 5, pp. 1610–1617, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Bab-Dinitz, H. Shmuely, J. Maupin-Furlow, J. Eichler, and B. Shaanan, “Haloferax volcanii PitA: an example of functional interaction between the Pfam chlorite dismutase and antibiotic biosynthesis monooxygenase families?” Bioinformatics, vol. 22, no. 6, pp. 671–675, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Large, C. Stamme, C. Lange et al., “Characterization of a tightly controlled promoter of the halophilic archaeon Haloferax volcanii and its use in the analysis of the essential cct1 gene,” Molecular Microbiology, vol. 66, no. 5, pp. 1092–1106, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Suzuki, Y. Ikeuchi, S. Kimura et al., “Agmatine-conjugated cytidine in a tRNA anticodon is essential for AUA decoding in archaea,” Nature Chemical Biology, vol. 6, no. 4, pp. 277–282, 2010. View at Publisher · View at Google Scholar
  46. D. Mandal, C. Köhrer, D. Su et al., “Agmatidine, a modified cytidine in the anticodon of archaeal tRNA(Ile), base pairs with adenosine but not with guanosine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 7, pp. 2872–2877, 2010. View at Publisher · View at Google Scholar
  47. A. Soma, Y. Ikeuchi, S. Kanemasa et al., “An RNA-modifying enzyme that governs both the codon and amino acid specificities of isoleucine tRNA,” Molecular Cell, vol. 12, no. 3, pp. 689–698, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. B. El Yacoubi, B. Lyons, Y. Cruz et al., “The universal YrdC/Sua5 family is required for the formation of threonylcarbamoyladenosine in tRNA,” Nucleic Acids Research, vol. 37, no. 9, pp. 2894–2909, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Kaur, P. T. Van, C. R. Busch et al., “Coordination of frontline defense mechanisms under severe oxidative stress,” Molecular Systems Biology, vol. 6, article no. 393, 2010. View at Publisher · View at Google Scholar
  50. T. Baba, H.-C. Huan, K. Datsenko, B. L. Wanner, and H. Mori, “The applications of systematic in-frame, single-gene knockout mutant collection of Escherichia coli K-12,” Methods in Molecular Biology, vol. 416, pp. 183–194, 2007. View at Google Scholar · View at Scopus
  51. M. Durot, F. Le Fèvre, V. de Berardinis et al., “Iterative reconstruction of a global metabolic model of Acinetobacter baylyi ADP1 using high-throughput growth phenotype and gene essentiality data,” BMC Systems Biology, vol. 2, article no. 85, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Zhou, X.-H. Lei, B. R. Bochner, and B. L. Wanner, “Phenotype microArray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems,” Journal of Bacteriology, vol. 185, no. 16, pp. 4956–4972, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. B. R. Bochner, “Global phenotypic characterization of bacteria,” FEMS Microbiology Reviews, vol. 33, no. 1, pp. 191–205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. T. C. Fleischer, C. M. Weaver, K. J. McAfee, J. L. Jennings, and A. J. Link, “Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes,” Genes and Development, vol. 20, no. 10, pp. 1294–1307, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Grosjean, C. Gaspin, C. Marck, W. A. Decatur, and V. de Crécy-Lagard, “RNomics and Modomics in the halophilic archaea Haloferax volcanii: identification of RNA modification genes,” BMC Genomics, vol. 9, article no. 470, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. M. G. Gomez-Lorenzo, C. M. T. Spahn, R. K. Agrawal et al., “Three-dimensional cryo-electron microscopy localization of EF2 in the Saccharomyces cerevisiae 80S ribosome at 17.5 Å resolution,” EMBO Journal, vol. 19, no. 11, pp. 2710–2718, 2000. View at Google Scholar · View at Scopus
  57. B. G. Van Ness, J. B. Howard, and J. W. Bodley, “ADP-ribosylation of elongation factor 2 by diphtheria toxin. Isolation and properties of the novel ribosyl-amino acid and its hydrolysis products,” Journal of Biological Chemistry, vol. 255, no. 22, pp. 10717–10720, 1980. View at Google Scholar · View at Scopus
  58. B. G. Van Ness, J. B. Howard, and J. W. Bodley, “ADP-ribosylation of elongation factor 2 by diphtheria toxin. NMR spectra and proposed structures of ribosyl-diphthamide and its hydrolysis products,” Journal of Biological Chemistry, vol. 255, no. 22, pp. 10710–10716, 1980. View at Google Scholar · View at Scopus
  59. P. A. Ortiz, R. Ulloque, G. K. Kihara, H. Zheng, and T. G. Kinzy, “Translation elongation factor 2 anticodon mimicry domain mutants affect fidelity and diphtheria toxin resistance,” Journal of Biological Chemistry, vol. 281, no. 43, pp. 32639–32648, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. C.-M. Chen and R. R. Behringer, “Ovca1 regulates cell proliferation, embryonic development, and tumorigenesis,” Genes and Development, vol. 18, no. 3, pp. 320–332, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. T. R. Webb, S. H. Cross, L. McKie et al., “Diphthamide modification of eEF2 requires a J-domain protein and is essential for normal development,” Journal of Cell Science, vol. 121, no. 19, pp. 3140–3145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. B. S. Laursen, I. Siwanowicz, G. Larigauderie et al., “Characterization of mutations in the GTP-binding domain of IF2 resulting in cold-sensitive growth of Escherichia coli,” Journal of Molecular Biology, vol. 326, no. 2, pp. 543–551, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. Z. Zhou and M. P. Deutscher, “An essential function for the phosphate-dependent exoribonucleases RNase PH and polynucleotide phosphorylase,” Journal of Bacteriology, vol. 179, no. 13, pp. 4391–4395, 1997. View at Google Scholar · View at Scopus
  64. Y. Zhang, X. Zhu, A. T. Torelli et al., “Diphthamide biosynthesis requires an organic radical generated by an iron-sulphur enzyme,” Nature, vol. 465, no. 7300, pp. 891–896, 2010. View at Publisher · View at Google Scholar
  65. L. Jovine, S. Djordjevic, and D. Rhodes, “The crystal structure of yeast phenylalanine tRNA at 2.0 Å resolution: cleavage by Mg2+ in 15-year old crystals,” Journal of Molecular Biology, vol. 301, no. 2, pp. 401–414, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Shi and P. B. Moore, “The crystal structure of yeast phenylalanine tRNA at 1.93 Å resolution: a classic structure revisited,” RNA, vol. 6, no. 8, pp. 1091–1105, 2000. View at Publisher · View at Google Scholar · View at Scopus
  67. R. Oliva, A. Tramontano, and L. Cavallo, “Mg2+ binding and archaeosine modification stabilize the G15-C48 Levitt base pair in tRNAs,” RNA, vol. 13, no. 9, pp. 1427–1436, 2007. View at Publisher · View at Google Scholar · View at Scopus