Molecular Biology and Evolution, Vol 16, 1586-1598, Copyright © 1999 by Society for Molecular Biology and Evolution
MA Clark, NA Moran and P Baumann
A major limitation on ability to reconstruct bacterial evolution is the
lack of dated ancestors that might be used to evaluate and calibrate
molecular clocks. Vertically transmitted symbionts that have cospeciated
with animal hosts offer a firm basis for calibrating sequence evolution in
bacteria, since fossils of the hosts can be used to date divergence events.
Sequences for a functionally diverse set of genes have been obtained for
bacterial endosymbionts (Buchnera) from two pairs of aphid host species,
each pair diverging 50-70 MYA. Using these dates and estimated numbers of
Buchnera generations per year, we calculated rates of base substitution for
neutral and selected sites of protein-coding genes and overall rates for
rRNA genes. Buchnera shows homogeneity among loci with regard to synonymous
rate. The Buchnera synonymous rate is about twice that for low-codon-bias
genes of Escherichia coli-Salmonella typhimurium on an absolute timescale,
and fourfold higher on a generational timescale. Nonsynonymous
substitutions show a greater rate disparity in favor of Buchnera, a result
consistent with a genomewide decrease in selection efficiency in Buchnera.
Ratios of synonymous to nonsynonymous substitutions differ for the two
pairs of Buchnera, indicating that selection efficiency varies among
lineages. Like numerous other intracellular bacteria, such as Rickettsia
and Wolbachia, Buchnera has accumulated amino acids with codons rich in A
or T. Phylogenetic reconstruction of amino acid replacements indicates that
replacements yielding increased A + T predominated early in the evolution
of Buchnera, with the trend slowing or stopping during the last 50 Myr.
This suggests that base composition in Buchnera has approached a limit
enforced by selective constraint acting on protein function.
ORIGINAL ARTICLE
Sequence evolution in bacterial endosymbionts having extreme base compositions
Microbiology Section, University of California, Davis, USA.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  C. Conord, L. Despres, A. Vallier, S. Balmand, C. Miquel, S. Zundel, G. Lemperiere, and A. Heddi Long-Term Evolutionary Stability of Bacterial Endosymbiosis in Curculionoidea: Additional Evidence of Symbiont Replacement in the Dryophthoridae Family Mol. Biol. Evol., May 1, 2008; 25(5): 859 - 868. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. P. Andam, S. J. Mondo, and M. A. Parker Monophyly of nodA and nifH Genes across Texan and Costa Rican Populations of Cupriavidus Nodule Symbionts Appl. Envir. Microbiol., July 15, 2007; 73(14): 4686 - 4690. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Slominski, J. Calkiewicz, P. Golec, G. Wegrzyn, and B. Wrobel Plasmids derived from Gifsy-1/Gifsy-2, lambdoid prophages contributing to the virulence of Salmonella enterica serovar Typhimurium: implications for the evolution of replication initiation proteins of lambdoid phages and enterobacteria Microbiology, June 1, 2007; 153(6): 1884 - 1896. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. N. Khachane, K. N. Timmis, and V. A. P. Martins dos Santos Dynamics of Reductive Genome Evolution in Mitochondria and Obligate Intracellular Microbes Mol. Biol. Evol., February 1, 2007; 24(2): 449 - 456. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Rasgon, X. Ren, and M. Petridis Can Anopheles gambiae Be Infected with Wolbachia pipientis? Insights from an In Vitro System Appl. Envir. Microbiol., December 1, 2006; 72(12): 7718 - 7722. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Perez-Brocal, R. Gil, S. Ramos, A. Lamelas, M. Postigo, J. M. Michelena, F. J. Silva, A. Moya, and A. Latorre A Small Microbial Genome: The End of a Long Symbiotic Relationship? Science, October 13, 2006; 314(5797): 312 - 313. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Mavromatis, C. K. Doyle, A. Lykidis, N. Ivanova, M. P. Francino, P. Chain, M. Shin, S. Malfatti, F. Larimer, A. Copeland, et al. The Genome of the Obligately Intracellular Bacterium Ehrlichia canis Reveals Themes of Complex Membrane Structure and Immune Evasion Strategies J. Bacteriol., June 1, 2006; 188(11): 4015 - 4023. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Huerta, J. Collado-Vides, and M. P. Francino Positional Conservation of Clusters of Overlapping Promoter-Like Sequences in Enterobacterial Genomes Mol. Biol. Evol., May 1, 2006; 23(5): 997 - 1010. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Klasson and S. G. E. Andersson Strong Asymmetric Mutation Bias in Endosymbiont Genomes Coincide with Loss of Genes for Replication Restart Pathways Mol. Biol. Evol., May 1, 2006; 23(5): 1031 - 1039. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Nei Selectionism and Neutralism in Molecular Evolution Mol. Biol. Evol., December 1, 2005; 22(12): 2318 - 2342. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. H. Degnan, A. B. Lazarus, and J. J. Wernegreen Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects Genome Res., August 1, 2005; 15(8): 1023 - 1033. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Belda, A. Moya, and F. J. Silva Genome Rearrangement Distances and Gene Order Phylogeny in {gamma}-Proteobacteria Mol. Biol. Evol., June 1, 2005; 22(6): 1456 - 1467. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. T. Herbeck, P. H. Degnan, and J. J. Wernegreen Nonhomogeneous Model of Sequence Evolution Indicates Independent Origins of Primary Endosymbionts Within the Enterobacteriales ({gamma}-Proteobacteria) Mol. Biol. Evol., March 1, 2005; 22(3): 520 - 532. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. D. Shoemaker, K. A. Dyer, M. Ahrens, K. McAbee, and J. Jaenike Decreased Diversity but Increased Substitution Rate in Host mtDNA as a Consequence of Wolbachia Endosymbiont Infection Genetics, December 1, 2004; 168(4): 2049 - 2058. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Gomez-Valero, A. Latorre, and F. J. Silva The Evolutionary Fate of Nonfunctional DNA in the Bacterial Endosymbiont Buchnera aphidicola Mol. Biol. Evol., November 1, 2004; 21(11): 2172 - 2181. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Gomez-Valero, M. Soriano-Navarro, V. Perez-Brocal, A. Heddi, A. Moya, J. M. Garcia-Verdugo, and A. Latorre Coexistence of Wolbachia with Buchnera aphidicola and a Secondary Symbiont in the Aphid Cinara cedri J. Bacteriol., October 1, 2004; 186(19): 6626 - 6633. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Lefevre, H. Charles, A. Vallier, B. Delobel, B. Farrell, and A. Heddi Endosymbiont Phylogenesis in the Dryophthoridae Weevils: Evidence for Bacterial Replacement Mol. Biol. Evol., June 1, 2004; 21(6): 965 - 973. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Canback, I. Tamas, and S. G. E. Andersson A Phylogenomic Study of Endosymbiotic Bacteria Mol. Biol. Evol., June 1, 2004; 21(6): 1110 - 1122. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Sabater-Munoz, R. C. H. J. van Ham, A. Moya, F. J. Silva, and A. Latorre Evolution of the Leucine Gene Cluster in Buchnera aphidicola: Insights from Chromosomal Versions of the Cluster J. Bacteriol., May 1, 2004; 186(9): 2646 - 2654. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Rispe, F. Delmotte, R. C.H.J. van Ham, and A. Moya Mutational and Selective Pressures on Codon and Amino Acid Usage in Buchnera, Endosymbiotic Bacteria of Aphids Genome Res., January 1, 2004; 14(1): 44 - 53. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. T. Herbeck, D. J. Funk, P. H. Degnan, and J. J. Wernegreen A Conservative Test of Genetic Drift in the Endosymbiotic Bacterium Buchnera: Slightly Deleterious Mutations in the Chaperonin groEL Genetics, December 1, 2003; 165(4): 1651 - 1660. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. T. Herbeck, D. P. Wall, and J. J. Wernegreen Gene expression level influences amino acid usage, but not codon usage, in the tsetse fly endosymbiont Wigglesworthia Microbiology, September 1, 2003; 149(9): 2585 - 2596. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Woolfit and L. Bromham Increased Rates of Sequence Evolution in Endosymbiotic Bacteria and Fungi with Small Effective Population Sizes Mol. Biol. Evol., September 1, 2003; 20(9): 1545 - 1555. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. J. Wernegreen, P. H. Degnan, A. B. Lazarus, C. Palacios, and S. R. Bordenstein Genome Evolution in an Insect Cell: Distinct Features of an Ant-Bacterial Partnership Biol. Bull., April 1, 2003; 204(2): 221 - 231. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. C. H. J. van Ham, J. Kamerbeek, C. Palacios, C. Rausell, F. Abascal, U. Bastolla, J. M. Fernandez, L. Jimenez, M. Postigo, F. J. Silva, et al. Reductive genome evolution in Buchnera aphidicola PNAS, January 21, 2003; 100(2): 581 - 586. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Itoh, W. Martin, and M. Nei Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts PNAS, October 1, 2002; 99(20): 12944 - 12948. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Palacios and J. J. Wernegreen A Strong Effect of AT Mutational Bias on Amino Acid Usage in Buchnera is Mitigated at High-Expression Genes Mol. Biol. Evol., September 1, 2002; 19(9): 1575 - 1584. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Parker, B. Lafay, J. J. Burdon, and P. van Berkum Conflicting phylogeographic patterns in rRNA and nifD indicate regionally restricted gene transfer in Bradyrhizobium Microbiology, August 1, 2002; 148(8): 2557 - 2565. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Baumann, M. L. Thao, J. M. Hess, M. W. Johnson, and P. Baumann The Genetic Properties of the Primary Endosymbionts of Mealybugs Differ from Those of Other Endosymbionts of Plant Sap-Sucking Insects Appl. Envir. Microbiol., July 1, 2002; 68(7): 3198 - 3205. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Fares, E. Barrio, B. Sabater-Munoz, and A. Moya The Evolution of the Heat-Shock Protein GroEL from Buchnera, the Primary Endosymbiont of Aphids, Is Governed by Positive Selection Mol. Biol. Evol., July 1, 2002; 19(7): 1162 - 1170. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Tamas, L. Klasson, B. Canback, A. K. Naslund, A.-S. Eriksson, J. J. Wernegreen, J. P. Sandstrom, N. A. Moran, and S. G. E. Andersson 50 Million Years of Genomic Stasis in Endosymbiotic Bacteria Science, June 28, 2002; 296(5577): 2376 - 2379. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Graur and T. Pupko The Permian Bacterium that Isn't Mol. Biol. Evol., June 1, 2001; 18(6): 1143 - 1146. [Full Text]
|
|
|
|
|
|
D. J. Funk, J. J. Wernegreen, and N. A. Moran Intraspecific Variation in Symbiont Genomes: Bottlenecks and the Aphid-Buchnera Association Genetics, February 1, 2001; 157(2): 477 - 489. [Abstract] [Full Text]
|
|
|
|
|
|
J. J. Wernegreen and N. A. Moran Vertical Transmission of Biosynthetic Plasmids in Aphid Endosymbionts (Buchnera) J. Bacteriol., January 15, 2001; 183(2): 785 - 790. [Abstract] [Full Text]
|
|
|
|
|
|
M. L. Thao, N. A. Moran, P. Abbot, E. B. Brennan, D. H. Burckhardt, and P. Baumann Cospeciation of Psyllids and Their Primary Prokaryotic Endosymbionts Appl. Envir. Microbiol., July 1, 2000; 66(7): 2898 - 2905. [Abstract] [Full Text]
|
|
|
|
|
|
J. J. Wernegreen, H. Ochman, I. B. Jones, and N. A. Moran Decoupling of Genome Size and Sequence Divergence in a Symbiotic Bacterium J. Bacteriol., July 1, 2000; 182(13): 3867 - 3869. [Abstract] [Full Text]
|
|