Skip to main content
Genetics logoLink to Genetics
. 2003 Dec;165(4):1651–1660. doi: 10.1093/genetics/165.4.1651

A conservative test of genetic drift in the endosymbiotic bacterium Buchnera: slightly deleterious mutations in the chaperonin groEL.

Joshua T Herbeck 1, Daniel J Funk 1, Patrick H Degnan 1, Jennifer J Wernegreen 1
PMCID: PMC1462895  PMID: 14704156

Abstract

The obligate endosymbiotic bacterium Buchnera aphidicola shows elevated rates of sequence evolution compared to free-living relatives, particularly at nonsynonymous sites. Because Buchnera experiences population bottlenecks during transmission to the offspring of its aphid host, it is hypothesized that genetic drift and the accumulation of slightly deleterious mutations can explain this rate increase. Recent studies of intraspecific variation in Buchnera reveal patterns consistent with this hypothesis. In this study, we examine inter- and intraspecific nucleotide variation in groEL, a highly conserved chaperonin gene that is constitutively overexpressed in Buchnera. Maximum-likelihood estimates of nonsynonymous substitution rates across Buchnera species are strikingly low at groEL compared to other loci. Despite this evidence for strong purifying selection on groEL, our intraspecific analysis of this gene documents reduced synonymous polymorphism, elevated nonsynonymous polymorphism, and an excess of rare alleles relative to the neutral expectation, as found in recent studies of other Buchnera loci. Comparisons with Escherichia coli generally show patterns predicted by their differences in N(e). The sum of these observations is not expected under relaxed or balancing selection, selective sweeps, or increased mutation rate. Rather, they further support the hypothesis that drift is an important force driving accelerated protein evolution in this obligate mutualist.

Full Text

The Full Text of this article is available as a PDF (107.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abbot P., Moran N. A. Extremely low levels of genetic polymorphism in endosymbionts (Buchnera) of aphids (Pemphigus). Mol Ecol. 2002 Dec;11(12):2649–2660. doi: 10.1046/j.1365-294x.2002.01646.x. [DOI] [PubMed] [Google Scholar]
  2. Akman Leyla, Yamashita Atsushi, Watanabe Hidemi, Oshima Kenshiro, Shiba Tadayoshi, Hattori Masahira, Aksoy Serap. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet. 2002 Sep 3;32(3):402–407. doi: 10.1038/ng986. [DOI] [PubMed] [Google Scholar]
  3. Bergthorsson U., Ochman H. Heterogeneity of genome sizes among natural isolates of Escherichia coli. J Bacteriol. 1995 Oct;177(20):5784–5789. doi: 10.1128/jb.177.20.5784-5789.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bochkareva E. S., Lissin N. M., Girshovich A. S. Transient association of newly synthesized unfolded proteins with the heat-shock GroEL protein. Nature. 1988 Nov 17;336(6196):254–257. doi: 10.1038/336254a0. [DOI] [PubMed] [Google Scholar]
  5. Boyd E. F., Nelson K., Wang F. S., Whittam T. S., Selander R. K. Molecular genetic basis of allelic polymorphism in malate dehydrogenase (mdh) in natural populations of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1280–1284. doi: 10.1073/pnas.91.4.1280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brookfield J. F., Sharp P. M. Neutralism and selectionism face up to DNA data. Trends Genet. 1994 Apr;10(4):109–111. doi: 10.1016/0168-9525(94)90201-1. [DOI] [PubMed] [Google Scholar]
  7. Brynnel E. U., Kurland C. G., Moran N. A., Andersson S. G. Evolutionary rates for tuf genes in endosymbionts of aphids. Mol Biol Evol. 1998 May;15(5):574–582. doi: 10.1093/oxfordjournals.molbev.a025958. [DOI] [PubMed] [Google Scholar]
  8. Clark M. A., Baumann L., Thao M. L., Moran N. A., Baumann P. Degenerative minimalism in the genome of a psyllid endosymbiont. J Bacteriol. 2001 Mar;183(6):1853–1861. doi: 10.1128/JB.183.6.1853-1861.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clark M. A., Moran N. A., Baumann P. Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol Biol Evol. 1999 Nov;16(11):1586–1598. doi: 10.1093/oxfordjournals.molbev.a026071. [DOI] [PubMed] [Google Scholar]
  10. Dauga Catherine. Evolution of the gyrB gene and the molecular phylogeny of Enterobacteriaceae: a model molecule for molecular systematic studies. Int J Syst Evol Microbiol. 2002 Mar;52(Pt 2):531–547. doi: 10.1099/00207713-52-2-531. [DOI] [PubMed] [Google Scholar]
  11. Fares Mario A., Ruiz-González Mario X., Moya Andrés, Elena Santiago F., Barrio Eladio. Endosymbiotic bacteria: groEL buffers against deleterious mutations. Nature. 2002 May 23;417(6887):398–398. doi: 10.1038/417398a. [DOI] [PubMed] [Google Scholar]
  12. Fares Mario Ali, Barrio Eladio, Sabater-Muñoz Beatriz, Moya Andrés. The evolution of the heat-shock protein GroEL from Buchnera, the primary endosymbiont of aphids, is governed by positive selection. Mol Biol Evol. 2002 Jul;19(7):1162–1170. doi: 10.1093/oxfordjournals.molbev.a004174. [DOI] [PubMed] [Google Scholar]
  13. Fayet O., Ziegelhoffer T., Georgopoulos C. The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol. 1989 Mar;171(3):1379–1385. doi: 10.1128/jb.171.3.1379-1385.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fu Y. X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997 Oct;147(2):915–925. doi: 10.1093/genetics/147.2.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Funk D. J., Helbling L., Wernegreen J. J., Moran N. A. Intraspecific phylogenetic congruence among multiple symbiont genomes. Proc Biol Sci. 2000 Dec 22;267(1461):2517–2521. doi: 10.1098/rspb.2000.1314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Funk D. J., Wernegreen J. J., Moran N. A. Intraspecific variation in symbiont genomes: bottlenecks and the aphid-buchnera association. Genetics. 2001 Feb;157(2):477–489. doi: 10.1093/genetics/157.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gil Rosario, Sabater-Muñoz Beatriz, Latorre Amparo, Silva Francisco J., Moya Andrés. Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci U S A. 2002 Mar 19;99(7):4454–4458. doi: 10.1073/pnas.062067299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Guttman D. S., Dykhuizen D. E. Detecting selective sweeps in naturally occurring Escherichia coli. Genetics. 1994 Dec;138(4):993–1003. doi: 10.1093/genetics/138.4.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hartl D. L., Moriyama E. N., Sawyer S. A. Selection intensity for codon bias. Genetics. 1994 Sep;138(1):227–234. doi: 10.1093/genetics/138.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hasegawa M., Cao Y., Yang Z. Preponderance of slightly deleterious polymorphism in mitochondrial DNA: nonsynonymous/synonymous rate ratio is much higher within species than between species. Mol Biol Evol. 1998 Nov;15(11):1499–1505. doi: 10.1093/oxfordjournals.molbev.a025877. [DOI] [PubMed] [Google Scholar]
  22. Herzer P. J., Inouye S., Inouye M., Whittam T. S. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol. 1990 Nov;172(11):6175–6181. doi: 10.1128/jb.172.11.6175-6181.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Itoh Takeshi, Martin William, Nei Masatoshi. Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc Natl Acad Sci U S A. 2002 Sep 16;99(20):12944–12948. doi: 10.1073/pnas.192449699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kreitman M. Methods to detect selection in populations with applications to the human. Annu Rev Genomics Hum Genet. 2000;1:539–559. doi: 10.1146/annurev.genom.1.1.539. [DOI] [PubMed] [Google Scholar]
  25. Lambert J. D., Moran N. A. Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4458–4462. doi: 10.1073/pnas.95.8.4458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Matsumoto K., Morioka M., Ishikawa H. Phosphocarrier proteins in an intracellular symbiotic bacterium of aphids. J Biochem. 1999 Sep;126(3):578–583. doi: 10.1093/oxfordjournals.jbchem.a022489. [DOI] [PubMed] [Google Scholar]
  27. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  28. Milkman R. Electrophoretic variation in Escherichia coli from natural sources. Science. 1973 Dec 7;182(4116):1024–1026. doi: 10.1126/science.182.4116.1024. [DOI] [PubMed] [Google Scholar]
  29. Mira A., Moran N. A. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb Ecol. 2002 Jun 28;44(2):137–143. doi: 10.1007/s00248-002-0012-9. [DOI] [PubMed] [Google Scholar]
  30. Moran N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2873–2878. doi: 10.1073/pnas.93.7.2873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Munson M. A., Baumann P., Clark M. A., Baumann L., Moran N. A., Voegtlin D. J., Campbell B. C. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol. 1991 Oct;173(20):6321–6324. doi: 10.1128/jb.173.20.6321-6324.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nachman M. W., Brown W. M., Stoneking M., Aquadro C. F. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics. 1996 Mar;142(3):953–963. doi: 10.1093/genetics/142.3.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nelson K., Selander R. K. Evolutionary genetics of the proline permease gene (putP) and the control region of the proline utilization operon in populations of Salmonella and Escherichia coli. J Bacteriol. 1992 Nov;174(21):6886–6895. doi: 10.1128/jb.174.21.6886-6895.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ochman H., Selander R. K. Standard reference strains of Escherichia coli from natural populations. J Bacteriol. 1984 Feb;157(2):690–693. doi: 10.1128/jb.157.2.690-693.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Palacios Carmen, Wernegreen Jennifer J. A strong effect of AT mutational bias on amino acid usage in Buchnera is mitigated at high-expression genes. Mol Biol Evol. 2002 Sep;19(9):1575–1584. doi: 10.1093/oxfordjournals.molbev.a004219. [DOI] [PubMed] [Google Scholar]
  36. Peek A. S., Vrijenhoek R. C., Gaut B. S. Accelerated evolutionary rate in sulfur-oxidizing endosymbiotic bacteria associated with the mode of symbiont transmission. Mol Biol Evol. 1998 Nov;15(11):1514–1523. doi: 10.1093/oxfordjournals.molbev.a025879. [DOI] [PubMed] [Google Scholar]
  37. Rand D. M., Dorfsman M., Kann L. M. Neutral and non-neutral evolution of Drosophila mitochondrial DNA. Genetics. 1994 Nov;138(3):741–756. doi: 10.1093/genetics/138.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rand D. M., Kann L. M. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol. 1996 Jul;13(6):735–748. doi: 10.1093/oxfordjournals.molbev.a025634. [DOI] [PubMed] [Google Scholar]
  39. Rand D. M., Weinreich D. M., Cezairliyan B. O. Neutrality tests of conservative-radical amino acid changes in nuclear- and mitochondrially-encoded proteins. Gene. 2000 Dec 30;261(1):115–125. doi: 10.1016/s0378-1119(00)00483-2. [DOI] [PubMed] [Google Scholar]
  40. Sharp P. M., Li W. H. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987 Feb 11;15(3):1281–1295. doi: 10.1093/nar/15.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Shigenobu S., Watanabe H., Hattori M., Sakaki Y., Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature. 2000 Sep 7;407(6800):81–86. doi: 10.1038/35024074. [DOI] [PubMed] [Google Scholar]
  42. Suzuki Yoshiyuki, Nei Masatoshi. Simulation study of the reliability and robustness of the statistical methods for detecting positive selection at single amino acid sites. Mol Biol Evol. 2002 Nov;19(11):1865–1869. doi: 10.1093/oxfordjournals.molbev.a004010. [DOI] [PubMed] [Google Scholar]
  43. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tamas Ivica, Klasson Lisa, Canbäck Björn, Näslund A. Kristina, Eriksson Ann-Sofie, Wernegreen Jennifer J., Sandström Jonas P., Moran Nancy A., Andersson Siv G. E. 50 million years of genomic stasis in endosymbiotic bacteria. Science. 2002 Jun 28;296(5577):2376–2379. doi: 10.1126/science.1071278. [DOI] [PubMed] [Google Scholar]
  45. Wernegreen J. J., Lazarus Adam B., Degnan Patrick H. Small genome of Candidatus Blochmannia, the bacterial endosymbiont of Camponotus, implies irreversible specialization to an intracellular lifestyle. Microbiology. 2002 Aug;148(Pt 8):2551–2556. doi: 10.1099/00221287-148-8-2551. [DOI] [PubMed] [Google Scholar]
  46. Wernegreen J. J., Moran N. A. Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol Biol Evol. 1999 Jan;16(1):83–97. doi: 10.1093/oxfordjournals.molbev.a026040. [DOI] [PubMed] [Google Scholar]
  47. Wernegreen J. J., Moran N. A. Vertical transmission of biosynthetic plasmids in aphid endosymbionts (Buchnera). J Bacteriol. 2001 Jan;183(2):785–790. doi: 10.1128/JB.183.2.785-790.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wernegreen J. J., Richardson A. O., Moran N. A. Parallel acceleration of evolutionary rates in symbiont genes underlying host nutrition. Mol Phylogenet Evol. 2001 Jun;19(3):479–485. doi: 10.1006/mpev.2001.0929. [DOI] [PubMed] [Google Scholar]
  49. Whittam T. S., Ochman H., Selander R. K. Multilocus genetic structure in natural populations of Escherichia coli. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1751–1755. doi: 10.1073/pnas.80.6.1751. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES