Degenerative evolution and functional diversification of type-III secretion systems in the insect endosymbiont Sodalis glossinidius

Molecular Biology and Evolution

Volumn 22, Issue 3, 2005, Pages 758-766

  Dale, Colin ^a   Jones, Tait ^a   Pontes, Mauricio ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Adaptive evolution; Neofunctionalization; Symbiosis; Type III secretion system

Indexed keywords

ARTICLE; BACTERIAL VIRULENCE; CELL LINE; DEGENERATION; ENDOSYMBIOSIS; EUKARYOTIC CELL; EVOLUTIONARY ADAPTATION; GENE; GENE EXPRESSION; GENETIC VARIABILITY; HOST CELL; INFECTION; INSECT; INSECT CELL; INSECT GENETICS; INVA GENE; MOLECULAR EVOLUTION; MUTANT; NONHUMAN; PATHOGENICITY; PHYLOGENY; POLYMERASE CHAIN REACTION; SECRETION; SEQUENCE HOMOLOGY; SODALIS GLOSSINIDIUS; SYMBIOSIS; TSETSE FLY; TYPE 3 SECRETION SYSTEM; YSAV GENE;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; EVOLUTION, MOLECULAR; GRAM-NEGATIVE BACTERIA; INSECTS; SYMBIOSIS;

EID: 14544278532     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi061     Document Type: Article

References (38)

1. Akman, L., R. V. Rio, C. B. Beard, and S. Aksoy. 2001. Genome size determination and coding capacity of Sodalis glossinidius, an enteric symbiont of tsetse flies, as revealed by hybridization to Escherichia coli gene arrays. J. Bacteriol. 183:4517-4525.
2. Aksoy, S., X. Chen, and V. Hypsa. 1997. Phylogeny and potential transmission routes of midgut-associated endosymbionts of tsetse (Diptera:Glossinidae). Insect Mol. Biol. 6:183-190.
3. Bronstein, P. A., E. A. Miao, and S. I. Miller. 2000. InvB is a type III secretion chaperone specific for SspA. J. Bacteriol. 182: 6638-6644.
4. Chang, J. H., A. K. Goel, S. R. Grant, and J. L. Dangl. 2004. Wake of the flood: ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria. Curr. Opin. Microbiol. 7:11-18.
5. Collazo, C. M., and J. E. Galan. 1997. The invasion-associated type-III protein secretion system in Salmonella: a review. Gene 192:51-59.
6. Collazo, C. M., M. K. Zierler, and J. E. Galan. 1995. Functional analysis of the Salmonella typhimurium invasion genes invI and invJ and identification of a target of the protein secretion apparatus encoded in the inv locus. Mol. Microbiol. 15: 25-38.
7. Cornells, G. R., and F. Van Gijsegem. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
8. Dale, C., and I. Maudlin. 1999. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int. J. Syst. Bacteriol. 49:267-275.
9. Dale, C., G. R. Plague, B. Wang, H. Ochman, and N. A. Moran. 2002. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc. Natl. Acad. Sci. USA 99:12397-12402.
10. Dale, C., S. A. Young, D. T. Haydon, and S. C. Welburn. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA. 98:1883-1888.
11. Foultier, B., P. Troisfontaines, S. Muller, F. R. Opperdoes, and G. R. Comelis. 2002. Characterization of the ysa pathogenicity locus in the chromosome of Yersinia enterocolitica and phylogeny analysis of type III secretion systems. J. Mol. Evol. 55:37-51.
12. Gingrich, J. C., D. M. Boehrer, and S. B. Basu. 1996. Partial CviJI digestion as an alternative approach to generate cosmid sublibraries for large-scale sequencing projects. Biotechniques 21:99-104.
13. Horn, M., A. Ollingro, S. Schmitz-Esser et al. (13 co-authors). 2004. Illuminating the evolutionary history of Chlamydiae. Science 304: 728-730.
14. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
15. Hughes, A. L. 1994. The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B Biol. Sci. 256:119-124.
16. Kaniga, K., D. Trollinger, and J. E. Galan. 1995. Homologues of the Shigella invasions ipaB and ipaC are required for Salmonella typhimurium entry into cultured cells. J. Bacteriol. 177:3965-3971.
17. Kelley, J. M., C. E. Fields, M. B. Craven, D. Bocskai, U. Kim, S. D. Rounsley, and M. D. Adams. 1999. High throughput direct end sequencing of BAC clones. Nucleic Acids Res. 27: 1539-1546.
18. Klein, J. R., T. F. Fahlen, and B. D. Jones. 2000. Transcriptional organization and function of invasion genes within Salmonella enterica serovar typhimurium pathogenicity island 1, including the prgH, prgI, prgJ, prgK, orgA, orgB, and orgC genes. Infect. Immun. 68:3368-3376.
19. Kubori, T., and J. E. Galan. 2002. Salmonella type III secretion-associated protein InvE controls translocation of effector proteins into host cells. J. Bacteriol. 184:4699-4708.
20. Kubori, T., A. Sukhan, S. I. Aizawa, and J. E. Galan. 2000. Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. Proc. Natl. Acad. Sci. USA. 97:10225-10230.
21. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245.
22. Lithwick, G., and H. Margalit. 2003. Hierarchy of sequence-dependent features associated with prokaryotic translation. Genome Res. 13:2665-2673.
23. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408.
24. Lukashin, A., and M. Borodovsky. 1998. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26:1107-1115.
25. Lynch, M., M. O'Hely, B. Walsh, and A. Force. 2001. Distribution of pathogenicity islands in Salmonella spp. Genetics 159: 1789-1804.
26. Marie, C., W. J. Broughton, and W. J. Deakin. 2001. Rhizobium type III secretion systems: legume charmers or alarmers? Curr. Opin. Plant Biol. 4:336-342.
27. Nei, M., and S. Kumar. 2000. Molecular evolution and phylogenetics. Oxford University Press, New York
28. Ochman, H., and E. A. Groisman. 1996. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Infect. Immun. 64:5410-5412.
29. Ohno, S. 1970. Evolution by gene duplication. Springer, Heidelberg.
30. Pema, N.T., G. Plunkett, V. Burland et al. (28 co-authors). 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529-533.
31. Posada, J., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
32. Ribeiro de Vasconcelosa, A. T., D. F. de Almeidab, M. Hungriac et al. (112 co-authors). 2003. The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability. Proc. Natl. Acad. Sci. USA 100:11660-11665.
33. Saier, M. H. 2004. Evolution of bacterial type III protein secretion systems. Trends Microbiol. 12:113-115.
34. Sukhan, A., T. Kubori, J. Wilson, and J. E. Galan. 2001. Genetic analysis of assembly of the Salmonella enterica serovar typhimurium type III secretion-associated needle complex. J. Bacteriol. 183:1159-1167.
35. Swofford, D. L. 2000. PAUP*: phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, Mass.
36. Walsh, B. 2003. Population-genetic models of the fates of duplicate genes. Genetica 118:279-294.
37. Waterman, S. R., and D. W. Holden. 2003. Wake of the flood: ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria. Cell. Microbiol. 5:501-511.
38. Zhou, D., and J. E. Galan, 2001. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Microbes Infect. 3:1293-1298.