Table of Contents
International Journal of Evolutionary Biology
Volume 2011, Article ID 781642, 10 pages
http://dx.doi.org/10.4061/2011/781642
Research Article

Parallel Evolution and Horizontal Gene Transfer of the pst Operon in Firmicutes from Oligotrophic Environments

1Departamento de Ecologia Evolutiva, Instituto de Ecologia, Universidad Nacional Autónoma de México, Apdo. Postal 70-275, Ciudad Universitaria, 04510 México D. F., Mexico
2Departamento de Ingeniería Genética, CINVESTAV Campus Guanajuato, Apdo. Postal 629, 36500 Irapuato, Mexico
3Departamento de Bioquimica, Facultad de Quimica, Universidad Nacional Autonoma de México, Apdo. Postal 70-275, Ciudad Universitaria, 04510 México D. F., Mexico

Received 22 October 2010; Accepted 22 December 2010

Academic Editor: Hiromi Nishida

Copyright © 2011 Alejandra Moreno-Letelier 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. S. G. Tetu, B. Brahamsha, D. A. Johnson et al., “Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102,” ISME Journal, vol. 3, no. 7, pp. 835–849, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. P. G. Falkowski, T. Fenchel, and E. F. Delong, “The microbial engines that drive earth's biogeochemical cycles,” Science, vol. 320, no. 5879, pp. 1034–1039, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. D. Papineau, “Global biogeochemical changes at both ends of the Proterozoic: insights from phosphorites,” Astrobiology, vol. 10, no. 2, pp. 165–181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. J. J. Elser, J. Watts, J. H. Schampel, and J. Farmer, “Early Cambrian food webs on a trophic knife-edge? A hypothesis and preliminary data from a modern stromatolite-based ecosystem.,” Ecology Letters, vol. 9, no. 3, pp. 295–303, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. J. J. Elser and A. Hamilton, “Stoichiometry and the new biology: the future is now,” PLoS Biology, vol. 5, no. 7, article e181, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. M. V. Zubkov, I. Mary, E. M. S. Woodward et al., “Microbial control of phosphate in the nutrient-depleted North Atlantic subtropical gyre,” Environmental Microbiology, vol. 9, no. 8, pp. 2079–2089, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. D. B. Rusch, A. L. Halpern, G. Sutton et al., “The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific,” PLoS Biology, vol. 5, no. 3, article e77, 2007. View at Publisher · View at Google Scholar
  8. M. M. Adams, M. R. Gómez-García, A. R. Grossman, and D. Bhaya, “Phosphorus deprivation responses and phosphonate utilization in a thermophilic Synechococcus sp. from microbial mats,” Journal of Bacteriology, vol. 190, no. 24, pp. 8171–8184, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. L. D. Alcaraz, G. Olmedo, G. Bonilla et al., “The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 15, pp. 5803–5808, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Qi, Y. Kobayashi, and F. M. Hulett, “The pst operon of Bacillus subtilis has a phosphate-regulated promoter and is involved in phosphate transport but not in regulation of the Pho regulon,” Journal of Bacteriology, vol. 179, no. 8, pp. 2534–2539, 1997. View at Google Scholar · View at Scopus
  11. A. C. Martiny, M. L. Coleman, and S. W. Chisholm, “Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 33, pp. 12552–12557, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Aguena and B. Spira, “Transcriptional processing of the pst operon of Escherichia coli,” Current Microbiology, vol. 58, no. 3, pp. 264–267, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. A. C. Martiny, A. P. K. Tai, D. Veneziano, F. Primeau, and S. W. Chisholm, “Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus,” Environmental Microbiology, vol. 11, no. 4, pp. 823–832, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Sebastian and J. W. Ammerman, “The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA,” ISME Journal, vol. 3, no. 5, pp. 563–572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Aguena, E. Yagil, and B. Spira, “Transcriptional analysis of the pst operon of Escherichia coli,” Molecular Genetics and Genomics, vol. 268, no. 4, pp. 518–524, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. N. E. E. Allenby, N. O'Connor, Z. Prágai et al., “Post-transcriptional regulation of the Bacillus subtilis pst operon encoding a phosphate-specific ABC transporter,” Microbiology, vol. 150, no. 8, pp. 2619–2628, 2004. View at Google Scholar · View at Scopus
  17. R. J. Fischer, S. Oehmcke, U. Meyer et al., “Transcription of the pst operon of Clostridium acetobutylicum is dependent on phosphate concentration and pH,” Journal of Bacteriology, vol. 188, no. 15, pp. 5469–5478, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Tomii and M. Kanehisa, “A comparative analysis of ABC transporters in complete microbial genomes,” Genome Research, vol. 8, no. 10, pp. 1048–1059, 1998. View at Google Scholar · View at Scopus
  19. A. L. Davidson, E. Dassa, C. Orelle, and J. Chen, “Structure, function, and evolution of bacterial ATP-binding cassette systems,” Microbiology and Molecular Biology Reviews, vol. 72, no. 2, pp. 317–364, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. A. C. Martiny, Y. Huang, and W. Li, “Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions,” Environmental Microbiology, vol. 11, no. 6, pp. 1340–1347, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Feingersch, M. T. Suzuki, M. Shmoish et al., “Microbial community genomics in eastern Mediterranean Sea surface waters,” ISME Journal, vol. 4, no. 1, pp. 78–87, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. B. A. S. Van Mooy, H. F. Fredricks, B. E. Pedler et al., “Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity,” Nature, vol. 458, no. 7234, pp. 69–72, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. J. J. Elser, J. H. Schampel, F. Garcia-Pichel et al., “Effects of phosphorus enrichment and grazing snails on modern stromatolitic microbial communities,” Freshwater Biology, vol. 50, no. 11, pp. 1808–1825, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Souza, L. E. Eguiarte, J. Siefert, and J. J. Elser, “Microbial endemism: does phosphorus limitation enhance speciation?” Nature Reviews Microbiology, vol. 6, no. 7, pp. 559–564, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. V. Souza, L. Espinosa-Asuar, A. E. Escalante et al., “An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 17, pp. 6565–6570, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Desnues, B. Rodriguez-Brito, S. Rayhawk et al., “Biodiversity and biogeography of phages in modern stromatolites and thrombolites,” Nature, vol. 452, no. 7185, pp. 340–343, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. L. D. Alcaraz, G. Moreno-Hagelsieb, L. E. Eguiarte, V. Souza, L. Herrera-Estrella, and G. Olmedo, “Understanding the evolutionary relationships and major traits of Bacillus through comparative genomics,” BMC Genomics, vol. 11, no. 1, article no. 332, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Breitbart, A. Hoare, A. Nitti et al., “Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Ciénegas, Mexico,” Environmental Microbiology, vol. 11, no. 1, pp. 16–34, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. B. M. Winsborough, E. Theriot, and D. B. Czarnecki, Diatoms on a Continental Island: Lazarus Species, Marine Disjuncts and other Endemic Diatoms of the Cuatro Ciénegas basin, Coahuila, México, University of Texas, Austin Tex, USA, 2008.
  30. W. L. Minkley, “Cuatro Cienegas fishes: research reviewd and a local test of diversity versus habitat size,” Journal of the Arizona-Nevada Academy of Science, vol. 19, pp. 13–21, 1984. View at Google Scholar
  31. E. W. Carson and T. E. Dowling, “Influence of hydrogeographic history and hybridization on the distribution of genetic variation in the pupfishes Cyprinodon atrorus and C. bifasciatus,” Molecular Ecology, vol. 15, no. 3, pp. 667–679, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. S. G. Johnson, “Age, phylogeography and population structure of the microendemic banded spring snail, Mexipyrgus churinceanus,” Molecular Ecology, vol. 14, no. 8, pp. 2299–2311, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Tobler and E. W. Carson, “Environmental variation, hybridization, and phenotypic diversification in Cuatro Ciénegas pupfishes,” Journal of Evolutionary Biology, vol. 23, no. 7, pp. 1475–1489, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Cerritos, P. Vinuesa, L. E. Eguiarte et al., “Bacillus coahuilensis sp. nov., a moderately halophilic species from a desiccation lagoon in the Cuatro Ciénegas Valley in Coahuila, Mexico,” International Journal of Systematic and Evolutionary Microbiology, vol. 58, no. 4, pp. 919–923, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Cerritos, L. E. Eguiarte, M. Avitia et al., “Diversity of culturable thermo-resistant aquatic bacteria along an environmental gradient in Cuatro Ciénegas, Coahuila, Mexico,” Antonie Van Leeuwenhoek, vol. 99, no. 2, pp. 303–318, 2010. View at Publisher · View at Google Scholar
  36. A. E. Escalante, L. E. Eguiarte, L. Espinosa-Asuar, L. J. Forney, A. M. Noguez, and V. Souza Saldivar, “Diversity of aquatic prokaryotic communities in the Cuatro Cienegas basin,” FEMS Microbiology Ecology, vol. 65, no. 1, pp. 50–60, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. F. U. Battistuzzi, A. Feijao, and S. B. Hedges, “A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land,” BMC Evolutionary Biology, vol. 4, article no. 44, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Maughan, “Rates of molecular evolution in bacteria are relatively constant despite spore dormancy,” Evolution, vol. 61, no. 2, pp. 280–288, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Kunst, N. Ogasawara, I. Moszer et al., “The complete genome sequence of the gram-positive bacterium Bacillus subtilis,” Nature, vol. 390, no. 6657, pp. 249–256, 1997. View at Publisher · View at Google Scholar
  40. M. J. Sanderson, “Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach,” Molecular Biology and Evolution, vol. 19, no. 1, pp. 101–109, 2002. View at Google Scholar · View at Scopus
  41. I. Ferrusquía-Villafranca, “Geología de México: una sinopsis,” in Diversidad biológica de México: orígenes y distribución, T. P. Ramamoorthy et al., Ed., Instituto de Biología UNAM, México D.F., 1998. View at Google Scholar
  42. R. C. Edgar, “MUSCLE: a multiple sequence alignment method with reduced time and space complexity,” BMC Bioinformatics, vol. 5, article no. 113, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Stamatakis, P. Hoover, and J. Rougemont, “A rapid bootstrap algorithm for the RAxML web servers,” Systematic Biology, vol. 57, no. 5, pp. 758–771, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Abascal, R. Zardoya, and D. Posada, “ProtTest: selection of best-fit models of protein evolution,” Bioinformatics, vol. 21, no. 9, pp. 2104–2105, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. T. L. Bailey and C. Elkan, “Fitting a mixture model by expectation maximization to discover motifs in biopolymers,” in Proceedings of the 2nd International Conference on Intelligent Systems for Molecular Biology, vol. 2, pp. 28–36, 1994. View at Scopus
  46. M. Tanabe, O. Mirza, T. Bertrand et al., “Structures of OppA and PstS from Yersinia pestis indicate variability of interactions with transmembrane domains,” Acta Crystallographica Section D, vol. 63, no. 11, pp. 1185–1193, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Eswar, B. Webb, M. A. Marti-Renom et al., “Comparative protein structure modeling using Modeller,” Current Protocols in Bioinformatics, vol. 5, pp. 5.6.1–5.6.30, 2006. View at Google Scholar · View at Scopus
  48. V. A. Ilyin, A. Abyzov, and C. M. Leslin, “Structural alignment of proteins by a novel TOPOFIT method, as a superimposition of common volumes at a topomax point,” Protein Science, vol. 13, no. 7, pp. 1865–1874, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Tamura, J. Dudley, M. Nei, and S. Kumar, “MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0,” Molecular Biology and Evolution, vol. 24, no. 8, pp. 1596–1599, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. A. L. Hughes, “Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level,” Heredity, vol. 99, no. 4, pp. 364–373, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Luecke and F. A. Quiocho, “High specificity of a phosphate transport protein determined by hydrogen bonds,” Nature, vol. 347, no. 6291, pp. 402–406, 1990. View at Publisher · View at Google Scholar · View at Scopus
  52. E. V. Koonin, Y. I. Wolf, and G. P. Karev, “The structure of the protein universe and genome evolution,” Nature, vol. 420, no. 6912, pp. 218–223, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. R. A. Goldstein, “The structure of protein evolution and the evolution of protein structure,” Current Opinion in Structural Biology, vol. 18, no. 2, pp. 170–177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Sánchez-Flores, E. Pérez-Rueda, and L. Segovia, “Protein homology detection and fold inference through multiple alignment entropy profiles,” Proteins: Structure, Function and Genetics, vol. 70, no. 1, pp. 248–256, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. R. Woods, D. Schneider, C. L. Winkworth, M. A. Riley, and R. E. Lenski, “Tests of parallel molecular evolution in a long-term experiment with Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 24, pp. 9107–9112, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. J. H. Yoon, I. G. Kim, K. H. Kang, T. K. Oh, and Y. H. Park, “Bacillus marisflavi sp. nov. and Bacillus aquimaris sp. nov., isolated from sea water of a tidal flat of the Yellow Sea in Korea,” International Journal of Systematic and Evolutionary Microbiology, vol. 53, no. 5, pp. 1297–1303, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Vega, T. Nyborg, M. Perrilliat, M. Montellanos-Ballesteros, S. R. S. Cevallos-Ferriz, and S. A. Quiroz-Barroso, Studies on Mexican Paleontology, Springer, Dordrecht, The Nederlands, 2006.