The evolutionary fate of nonfunctional DNA in the bacterial endosymbiont Buchnera aphidicola

Molecular Biology and Evolution

Volumn 21, Issue 11, 2004, Pages 2172-2181

  Gómez Valero, Laura ^a   Latorre, Amparo ^a   Silva, Francisco J ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Buchnera aphidicola; DNA loss; Gene disintegration; Genome reduction; Pseudogenes; Symbiosis

Indexed keywords

BACTERIAL DNA; SPACER DNA;

ACYRTHOSIPHON PISUM; APHID; ARTICLE; BAIZONGIA PISTACIA; BUCHNERA; BUCHNERA APHIDICOLA; ENDOSYMBIOSIS; ESCHERICHIA COLI; GENE INACTIVATION; GENOME SIZE; MOLECULAR EVOLUTION; NONHUMAN; PSEUDOGENE; SCHIZAPHIS GRAMINUM;

BUCHNERA; DNA; DNA, BACTERIAL; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE DELETION; GENOME, BACTERIAL; MODELS, GENETIC; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; TIME FACTORS;

ACYRTHOSIPHON; ACYRTHOSIPHON PISUM; APHIDIDAE; APHIDINAE; BACTERIA (MICROORGANISMS); BAIZONGIA; BUCHNERA APHIDICOLA; ESCHERICHIA COLI; NEGIBACTERIA; PEMPHIGINAE; PISTACIA; PISUM; PROKARYOTA; SCHIZAPHIS; SCHIZAPHIS GRAMINUM;

EID: 6344269329     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh232     Document Type: Article

References (58)

1. Akman, L., A. Yamashita, H. Watanabe, K. Oshima, T. Shiba, M. Hattori, and S. Aksoy. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402-407.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. H. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res. 25:3389-3402.
3. Andersson, J. O., and S. G. Andersson. 1999. Genome degradation is an ongoing process in Rickettsia. Mol. Biol. Evol. 16:1178-1191.
4. -. 2001. Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes. Mol. Biol. Evol. 18:829-839.
5. Andersson, S. G., and C. G. Kurland. 1998. Reductive evolution of resident genomes. Trends Microbiol. 6:263-268.
6. Andersson, S. G. E., A. Zomoropipour, J. O. Andersson, T. Sicheritz-Ponten, U. C. M. Alsmark, R. M. Podowski, A. K. Naslund, A.-S. Eriksson, H. Winklerh, and C. G. Kurland. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133-143.
7. Baumann, L., P. Baumann, N. A. Moran, J. Sandstrom, and M. L. Thao. 1999. Genetic characterization of plasmids containing genes encoding enzymes of leucine biosynthesis in endosymbionts (Buchnera) of aphids. J. Mol. Evol. 48:77-85.
8. Baumann, P., L. Baumann, C.-Y. Lai, and D. Rouhbakhs. 1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49:55-94.
9. Bergthorsson, U., and H. Ochman. 1998. Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol. Biol. Evol. 15:6-16.
10. Blumenstiel, J. P., D. L. Hartl, and E. R. Lozovsky. 2002. Patterns of insertion and deletion in contrasting chromatin domains. Mol. Biol. Evol. 19:2211-2225.
11. Bracho, A. M., D. Martinez-Torres, A. Moya, and A. Latorre. 1995. Discovery and molecular characterization of a plasmid localized in Buchnerasp. bacterial endosymbiont of the aphid Rhopalisiphum padi. J. Mol. Evol. 41:67-73.
12. Brynnel, E. U., C. G. Kurland, N. Moran, and S. G. E. Anderson. 1998. Evolutionary rates for tuf genes in endosymbionts of aphids. Mol. Biol. Evol. 15:574-582.
13. Chambaud, I., R. Heilig, S. Ferris et al. (12 co-authors). 2001. The complete genome sequence of the murine respiratory pathogen Mycoplasma pulmonis. Nucleic Acids Res. 29: 2145-2153.
14. Clark, M. A., L. Baumann, M. L. Thao, N. A. Moran, and P. Baumann. 2001. Degenerative minimalism in the genome of a psyllid endosymbiont. J. Bacteriol. 183:1853-1861.
15. Clark, M. A., N. A. Moran, and P. Baumann. 1999. Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol. Biol. Evol. 16:1586-1598.
16. Frank, A. C., H. Amiri, and S. G. E. Andersson. 2002. Genome deterioration: loss of repeated sequences and accumulation of junk DNA. Genetica. 115:1-12.
17. Fraser, C. M., J. D. Gocayne, O. White et al. (29 co-authors). 1995. The minimal gene complement of Mycoplasma genitaliun. Science 270:397-403.
18. Gil, R., B. Sabater-Munoz, A. Latorre, F. J. Silva, and A. Moya. 2002. Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc. Natl. Acad. Sci. USA 99:4454-4458.
19. Gil, R., F. J. Silva, E. Zientz et al. (13 co-authors). 2003. The genome sequence of Blochinannia floridanus: comparative analysis of reduced genomes. Proc. Natl. Acad. Sci. USA 100:9388-9393.
20. Gregory, T. R. 2004. Insertion-deletion biases and the evolution of genome size. Gene 324:15-34.
21. Gurvich O. L., P. V. Baranov, J. Zhou, A. W. Hammer, R. F. Gesteland, and J. F. Atkins. 2003. Sequences that direct significant levels of frameshifting are frequent in coding regions of Escherichia coli. EMBO J. 22:5941-5950.
22. Himmelreich, R., H. Hubert, H. Plagens, E. Pirkl, B. C. Li, and R. Hermann. 1996. Complete sequence analysis of the genome of the bacterium Mycoplasma pnewnoniae. Nucleic Acids Res. 24:4420-4449.
23. Kalman, S., W. Mitchell, R. Marathe, C. Lammel, J. Fan, R. W. Hyman, L. Olinger, J. Grimwood, R. W. Davis, and R. S. Stephens. 1999. Comparative genomes of Chlmydia pneumoniae and C. trachomatis. Nat. Genet. 21:385-389.
24. Komaki, K., and H. Ishikawa. 2000. Genomic copy number of intracellular bacterial symbionts of aphids varies in response to developmental stage and morph of their host. Insect. Biochem. Mol. Biol. 30:253-258.
25. Lai, C.-Y., L. Baumann, and P. Buumann. 1994. Amplification of trpEG: Adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc. Natl. Acad. Sci. USA 91: 3819-3823.
26. Lawrence, J. G., R. W. Hendrix, and S. Casjens. 2001. Where are the pseudogenes in bacterial genomes? Trends Microbiol. 9:535-540.
27. Mira, A., L. Klasson, and S. G. E. Andersson. 2002. Microbial genome evolution: sources of variability. Curr. Opin. Microbiol. 5:506-551.
28. Mira, A., and N. A. Moran. 2002. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44:137-143.
29. Mira, A., H. Ochman, and N. A. Moran. 2001. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17: 589-596.
30. Moran, N. A. 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93: 2873-2878.
31. -. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583-586.
32. Moran. N. A., and A. Mira. 2001. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol. 2:research0054.
33. Moran, N. A., M. A. Munson, P. Baumann, and H. Ishikawa. 1993. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc. R. Soc. Lond. B Biol. Sci. 253:167-171.
34. Moran, N. A., and J. J. Wernegreen. 2000. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15:321-326.
35. Ogata, H., S. Audic, P. Renesto-Audiffren et al. (11 co-authors). 2001. Mechanisms of evolution in Rickettsia conorii and R. prowaiekii. Science 293:2093-2098.
36. Petrov, D. A., and D. L. Haiti. 1998. High rate of DNA loss in the Drosophilo melanogaster and Drosophila virilis species groups. Mol. Biol. Evol. 15:293-302.
37. Petrov, D. A., T. A. Sangster, J. S. Johnston, D. L. Hartl, and K. L. Shaw. 2000. Evidence for DNA loss as a determinant of genome size. Science 287:1060-1062.
38. Remaudière, G., and M. Remaudière. 1997. Catalogue des Aphididae du Monde. Homoptera Aphidoidea. Institut National de la Recherche Agronomique, Paris.
39. Rocha, E. P., and A. Blanchard. 2002. Genomic repeats, genome plasticity and the dynamics of Mycoplasma evolution. Nucleic Acids Res. 30:2031-2042.
40. Rocha, E. P. C. 2003. An appraisal of the potential for illegitimate recombination in bacterial genomes and its consequences: from duplications to genome reduction. Genome Res. 13:1123-1132.
41. Rouhbakhsh, D., C. Lai, C. D. von Dohlen, M. A. Clark, L. Baumann, P. Baumann, N. A. Moran, and D. J. Voegtlin. 1996. The Tryptophan biosinthetic pathway of aphid endosymbionts (Buchnera): genetics and evolution of plasmid-associated anthranilate synthase (trpEG) within the Aphididae. J. Mol. Evol. 42:414-421.
42. Sabater-Munoz, B., L. Gomez-Valero, R. C. van Ham, F. J. Silva, and A. Latorre. 2002. Molecular characterization of the leucine cluster in Buchnera sp. strain PSY, a primary endosymbiont of the aphid Pemphigus spyrothecae. Appl. Environ. Microbiol. 68:2572-2575.
43. Sabater-Muñoz, B., R. C. H. J. van Ham, A. Moya, F. J. Silva, and A. Latorre. 2004. Evolution of the leucine gene cluster in Buchnera aphidicola. Insights from chromosomal versions. J. Bacteriol. 186:2646-2654.
44. Selosse, M., B. Albert, and B. Godelle. 2001. Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol. Evol. 16:135-141.
45. Shigenobu, S., H. Watanabe, M. Hattori, Y. Sakaki, and H. Ishikawa. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81-86.
46. Silva, F. J., A. Latorre, and A. Moya. 2001. Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet. 17:615-618.
47. -. 2003. Why are the genomes of endosymbiotic bacteria so stable? Trends Genet. 19:176-180.
48. Silva, F. J., R. C. H. J. van Ham, B. Sabater, and A. Latorre. 1998. Structure and evolution of the leucine plasmids carried by the endosymbiont (Buchnera aphidicola) from aphids of the family Aphididae. FEMS Microbiol. Lett. 168:43-49.
49. Stephens, R. S., S. Kalman, C. Lammel et al. (12 co-authors). 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759.
50. Tamas, I., L. Klasson, B. Canback, A. K. Naslund, A. S. Eriksson, J. J. Wernegreen, J. P. Sandstrom, N. A. Moran, and S. G. E. Andersson. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376-2379.
51. Tatusov, R. L., E. V. Koonin, and D. J. Lipman. 1997. A genomic perspective on protein families. Science. 278: 631-637.
52. van Ham, R. C. H. J., F. Gonzalez-Candelas, F. J. Silva, B. Sabater, A. Moya, and A. Latorre. 2000. Postsymbiotic plasmid acquisition and evolution of the repA1-replicon in Buchnera aphidicola. Proc. Natl. Acad. Sci. USA 97:10855-10860.
53. van Ham, R. C. H. J., J. Kamerbeek, C. Palacios et al. (16 co-authors). 2003. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. USA 100:581-586.
54. van Ham, R. C. H. J., D. Martinez-Torres, A. Moya, and A. Latorre. 1999. Plasmid-encoded anthranilate synthase (TrpEG) in Buchnera aphidicola from aphids of the family Pemphigidae. Appl. Environ. Microbiol. 65:117-125.
55. van Ham, R. C. H. J., A. Moya, and A. Latorre. 1997. Putative evolutionary origin of plasmids carrying the genes involved in leucine biosynthesis in Buchnera aphidicola (endosymbiont of aphids). J. Bacteriol 179:4768-4777.
56. von Dohlen, C. D., and N. A. Moran. 2000. Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alteration. Biol. J. Linn. Soc. 71: 689-717.
57. Wernegreen, J. J., H. Ochman, I. B. Jones, and N. A. Moran. 2000. Decoupling of genome size and sequence divergence in a symbiotic bacterium. J. Bacteriol. 182:3867-3869.
58. Wickham, S. A., and D. H. Lynn. 1990. Relations between growth-rate, cell-size, and DNA content in colpodean ciliates (Ciliophora, Colpodea). Eur. J. Protistol. 25:345-352.