Nonhomogeneous model of sequence evolution indicates independent origins of primary endosymbionts within the enterobacteriales (γ-Proteobacteria)

Molecular Biology and Evolution

Volumn 22, Issue 3, 2005, Pages 520-532

  Herbeck, Joshua T ^a,b   Degnan, Patrick H ^a   Wernegreen, Jennifer J ^a  

^a MARINE BIOLOGICAL LABORATORY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Buchnera; Enterobacteriales; Insect endosymbionts; Nucleotide composition; Phylogeny

Indexed keywords

CHAPERONIN; RNA 16S;

AMINO ACID SUBSTITUTION; ARTICLE; AT RICH SEQUENCE; BAYES THEOREM; BUCHNERA; DNA BASE COMPOSITION; ENDOSYMBIONT; ENDOSYMBIOSIS; ENTEROBACTER; ERWINIA; ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; HAEMOPHILUS INFLUENZAE; KLEBSIELLA PNEUMONIAE; MAXIMUM LIKELIHOOD METHOD; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PANTOEA AGGLOMERANS; PARSIMONY ANALYSIS; PHYLOGENY; PSEUDOMONAS AERUGINOSA; SALMONELLA TYPHIMURIUM; SERRATIA MARCESCENS; SHIGELLA FLEXNERI; VIBRIO CHOLERAE; WIGGLESWORTHIA; YERSINIA PESTIS;

ANIMALS; BASE SEQUENCE; ENTEROBACTERIACEAE; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GROEL PROTEIN; MODELS, GENETIC; PLANTS; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

EID: 14544293086     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi036     Document Type: Article

References (79)

1. Abbot, P., and N. A. Moran. 2002. Extremely low levels of genetic polymorphism in endosymbionts (Buchnera) of aphids (Pemphigus). Mol. Ecol. 11:2649-2660.
2. 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.
3. 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.
4. Baumann, P., N. A. Moran, and L. Baumann. 2000. Bacteriocyte-associated endosymbionts of insects. in M. Dworkin, ed. The prokaryotes, a handbook on the biology of bacteria; ecophysiology, isolation, identification, applications, Springer-Verlag, New York.
5. Bergthorsson, U., and H. Ochman. 1995. Heterogeneity of genome sizes among natural isolates of Escherichia coli. J. Bacteriol. 177:5784-5789.
6. Canbäck, B., I. Tamas, and S. G. E. Andersson. 2004. A phylogenomic study of endosymbiotic bacteria. Mol. Biol. Evol. 21:1110-1122.
7. Chang, B. S., and D. L. Campbell. 2000. Bias in phylogenetic reconstruction of vertebrate rhodopsin sequences. Mol. Biol. Evol. 17:1220-1231.
8. Charles, H., A. Heddi, and Y. Rahbe. 2001. A putative insect intracellular endosymbiont stem clade, within the Enterobacteriaceae, inferred from phylogenetic analysis based on a heterogeneous model of DNA evolution. C. R. Acad. Sci. III 324:489-494.
9. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
10. 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.
11. Cole, J., B. Chai, T. Marsh, R. Farris, Q. Wang, S. Kulam, S. Chandra, D. McGarrell, T. Schmidt, G. Garrity, and J. Tiedje. 2003. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 31:442-443.
12. Conant, G. C., and P. O. Lewis. 2001. Effects of nucleotide composition bias on the success of the parsimony criterion in phylogenetic inference. Mol. Biol. Evol. 18:1024-1033.
13. Dale, C., and I. Maudlin. 1999. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossinia morsitans morsitans. Int. J. Syst. Bacteriol. 49(Pt 1):267-275.
14. 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.
15. Daubin, V., N. A. Moran, and H. Ochman. 2003. Phylogenetics and the cohesion of bacterial genomes. Science 301:829-832.
16. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376.
17. -. 1988. Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Gen. 22:212-219.
18. Foster, P. G., L. S. Jermiin, and D. A. Hickey. 1997. Nucleotide composition bias affects amino acid content in proteins coded by animal mitochondria. J. Mol. Evol. 44:282-288.
19. Funk, D. J., J. J. Wernegreen, and N. A. Moran. 2001. Intraspecific variation in symbiont genomes: bottlenecks and the aphid-Buchnera association. Genetics 157:477-489.
20. Galtier, N., and M. Gouy. 1995. Inferring phylogenies from DNA sequences of unequal base compositions. Proc. Natl. Acad. Sci. USA 92:11317-11321.
21. -. 1998. Inferring pattern and process: maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis. Mol. Biol. Evol. 15:871-879.
22. Galtier, N., M. Gouy, and C. Gautier. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12:543-548.
23. Galtier, N., N. Tourasse, and M. Gouy. 1999. A nonhyperthermophilic common ancestor to extant life forms. Science 283:220-221.
24. 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.
25. Gil, R., F. J. Silva, E. Zientz, F. Delmotte, F. Gonzalez-Candelas, A. Latorre, C. Rausell, J. Kamerbeek, J. Gadau, B. Hölldobler, R. C. van Ham, R. Gross, and A. Moya. 2003. The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc. Natl. Acad. Sci. USA 100:9388-9393.
26. Graybeal, A. 1998. Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47:9-17.
27. Hasegawa, M., and T. Hashimoto. 1993. Ribosomal RNA trees misleading? Nature 361:23.
28. Hasegawa, M., T. Hashimoto, J. Adachi, N. Iwabe, and T. Miyata. 1993. Early branchings in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. J. Mol. Evol. 36:380-388.
29. Heddi, A., H. Charles, C. Khatchadourian, G. Bonnot, and P. Nardon. 1998. Molecular characterization of the principal symbiotic bacteria of the weevil Sitophilus oryzae: a peculiar G + C content of an endocytobiotic DNA. J. Mol. Evol. 47:52-61.
30. Herbeck, J. T., D. J. Funk, P. H. Degnan, and J. J. Wernegreen. 2003. A conservative test of genetic drift in the endosymbiotic bacterium Buchnera: slightly deleterious mutations in the chaperonin groEL. Genetics 165:1651-1660.
31. Herbeck, J. T., D. P. Wall, and J. J. Wernegreen. 2003. Gene expression level influences amino acid usage, but not codon usage, in the tsetse fly endosymbiont Wigglesworthia. Microbiology 149:2585-2596.
32. Hillis, D. M. 1998. Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst. Biol. 47:3-8.
33. Hillis, D. M., D. D. Pollock, J. A. McGuire, and D. J. Zwickl. 2003. Is sparse taxon sampling a problem for phylogenetic inference? Syst. Biol. 52:124-126.
34. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
35. Kishino, H., and M. Hasegawa. 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29:170-179.
36. Koga, R., T. Tsuchida, and T. Fukatsu. 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. Lond. Ser. B Biol. Sci. 270:2543-2550.
37. Lambert, J. D., and N. A. Moran. 1998. Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 95:4458-4462.
38. Lefèvre, C., H. Charles, A. Vallier, B. Delobel, B. Farrell, and A. Heddi. 2004. Endosymbiont phylogenesis in the Dryophthoridae weevils: evidence for bacterial replacement. Mol. Biol. Evol. 21:965-973.
39. Lerat, E., V. Daubin, and N. A. Moran. 2003. From gene trees to organismal phylogeny in the Prokaryotes: the case of the gamma-Proteobacteria. PLoS Biol. Oct. 1:E19.
40. Lawrence, J. G., H. Ochman, and D. L. Hartl. 1991. Molecular and evolutionary relationships among enteric bacteria. J. Gen. Microbiol. 137:1911-1921.
41. Lockhart, P. J., M. A. Steel, M. D. Hendy, and D. Penny. 1994. Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. 11:605-612.
42. Loomis, W. F., and D. W. Smith. 1990. Molecular phylogeny of Dictyostelium discoideum by protein sequence comparison. Proc. Natl. Acad. Sci. USA 87:9093-9097.
43. Maddison, D., and W. Maddison. 2002. MacClade: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, Mass.
44. Mira, A., H. Ochman, and N. A. Moran. 2001. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17:589-596.
45. Mira, A., and N. A. Moran. 2002. Estimating transmission size and population bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44:137-143.
46. Mooers, A. O., and E. C. Holmes. 2000. The evolution of base composition and phylogenetic inference. Trends Ecol. Evol. 15:365-369.
47. Moran, N. A. 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93:2873-2878.
48. -. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583-586.
49. Moran, N., and A. Telang. 1998. Bacteriocyte-associated symbionts of insects. Bioscience 48:295-304.
50. Moran, N. A., and A. Mira. 2001. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol. 2:RESEARCH0054.
51. Moran, N. A., and J. J. Wernegreen. 2000. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15:321-326.
52. Muto, A., and S. Osawa. 1987. The guanine and cytosine content of genomic DNA and bacterial evolution. Proc. Natl. Acad. Sci. USA 84:166-169.
53. Palacios, C., and J. J. Wernegreen. 2002. A strong effect of AT mutational bias on amino acid usage in Buchnera is mitigated at high expression genes. Mol. Biol. Evol. 19:1575-1584.
54. Pollock, D. D., D. J. Zwickl, J. A. McGuire, and D. M. Hillis. 2002. Increased taxon sampling is advantageous for phylogenetic inference. Syst. Biol. 51:664-671.
55. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
56. Rispe, C., F. Delmotte, R. C. van Ham, and A. Moya. 2004. Mutational and selective pressures on codon and amino acid usage in Buchnera, endosymbiotic bacteria of aphids. Genome Res. 14:44-53.
57. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
58. Rosenberg, M. S., and S. Kumar. 2003. Heterogeneity of nucleotide frequencies among evolutionary lineages and phylogenetic inference. Mol. Biol. Evol. 20:610-621.
59. Schröder, D., H. Deppisch, M. Obermayer, G. Krohne, E. Stackebrandt, B. Hölldobler, W. Goebel, and R. Gross. 1996. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol. Microbiol. 21:479-489.
60. 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.
61. Shimodaira, H., and M. Hasegawa. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16:1114-1116.
62. Singer, G. A., and D. A. Hickey. 2000. Nucleotide bias causes a genomewide bias in the amino acid composition of proteins. Mol. Biol. Evol. 17:1581-1588.
63. Spaulding, A. W., and C. D. von Dohlen. 1998. Phylogenetic characterization and molecular evolution of bacterial enndosymbionts in psyllids (Hemiptera: Sternorrhyncha). Mol. Biol. Evol. 15:1506-1513.
64. Sproer, C., U. Mendrock, J. Swiderski, E. Lang, and E. Stackebrandt. 1999. The phylogenetic position of Serratia, Buttiauxella and some other genera of the family Enterobacteriaceae. Int. J. Syst. Evol. Microbiol. 49:1433-1438.
65. Steel, M. A., P. J. Lockhart, and D. Penny. 1995. A frequency-dependent significance test for parsimony. Mol. Phylogenet. Evol. 4:64-71.
66. Sueoka, N. 1962. On the genetic basis of heterogeneity of DNA content. Proc. Natl. Acad. Sci. USA 48:582-592.
67. -. 1988. Directional mutation pressure and neutral molecular evolution. Proc. Natl. Acad. Sci. USA 85:2653-2657.
68. -. 1992. Directional mutation pressure, selective constraints, and genetic equilibria. J. Mol. Evol. 34:95-114.
69. Swofford, D. L. 2002. PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland, Mass.
70. Tamas, I., L. Klasson L, B. Canbäck, A. K. Naslund, A. S. Eriksson, J. J. Wernegreen, J. P. Sandstrom, N. A. Moran, and S. G. Andersson. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376-2379.
71. Tamura, K. 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C content biases. Mol. Biol. Evol. 9:678-687.
72. Tarrio, R., F. Rodriguez-Trelles, and F. J. Ayala. 2001. Shared nucleotide composition biases among species and their impact on phylogenetic reconstructions of the Drosophilidae. Mol. Biol. Evol. 18:1464-1473.
73. Tourasse, N. J., and W. H. Li. 1999. Performance of the relative-rate test under nonstationary models of nucleotide substitution. Mol. Biol. Evol. 16:1068-1078.
74. Van Ham, R. C., J. Kamerbeek, C. Palacios, C. Rausell, F. Abascal, U. Bastolla, J. M. Fernandez, L. Jimenez, M. Postigo, F. J. Silva et al. (16 co-authors). 2003. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. USA 100:581-586.
75. Wernegreen, J. J., A. B. Lazarus, and P. H. Degnan. 2002. Small genome of Candidatus Blochmannia, the bacterial endosymbiont of Camponotus, implies irreversible specialization to an intracellular lifestyle. Microbiology 148:2551-2556.
76. Wernegreen, J. J., and N. A. Moran. 1999. Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol. Biol. Evol. 16:83-97.
77. Wertz, J. E., C. Goldstone, D. M. Gordon, and M. A. Riley. 2003. A molecular phylogeny of enteric bacteria and implications for a bacterial species concept. J. Evol. Biol. 16:1236-1248.
78. Woolfit, M., and L. Bromham. 2003. Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol. Biol. Evol. 20:1545-155.
79. Yang, Z. 1993. Maximum-likelihood estimation of phylogeny from DNA when substitution rates differ over sites. Mol. Biol. Evol. 10:1396-1401.