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13 - Lessons in Evolution from Genome Reduction in Endosymbionts

from PART IV - Interkingdom Transfer and Endosymbiosis

Published online by Cambridge University Press:  16 September 2009

By
Andrés Moya  and
Amparo Latorre
Edited by
Michael Hensel  and
Herbert Schmidt
Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
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Summary

INTRODUCTION

Intracellular bacteria (symbionts and parasites) are characterized by a genome reduction syndrome that, when compared to their free-living relatives, leads us to the conclusion that they are evolving anomalously. Is this right? The notion of anomaly has an anthropocentric connotation, and from such a viewpoint we cannot state that genome reduction is an evolutionary anomaly; likewise we cannot state that parasitic organisms represent a degenerate stage of evolution as compared to their non-parasitic ancestors. By contrast, we can affirm that they represent an anomaly if we are unable to explain their origin and evolution, given there is no suitable theory to explain both the increase in genome size and evolutionary complexity as well as the genome reduction process in endosymbionts. The question is: Do we have such a theory? In the past few years Michel Lynch and collaborators have published a series of papers on this particular issue, trying to integrate the evolution of genome size and concomitantly genome complexity of prokaryotes and eukaryotes into a single theoretical framework following the basic principles of population genetics.

In this chapter, we would like to deal with how basic principles, such as mutation, selection, and effective population size, can give us an acceptable explanation, empirically founded, of the genome reduction process in endosymbiotic bacteria. We propose a model that both explains the huge transformation of endosymbiotic genomes at nucleotide level and accounts for genome reduction.

Type
Chapter
Information
Horizontal Gene Transfer in the Evolution of Pathogenesis , pp. 317 - 334
Publisher: Cambridge University Press
Print publication year: 2008

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References

Birky, C.W. (2001). The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet, 35, 125–48.CrossRefGoogle ScholarPubMed
Birky, C.W., Maruyama, T., and Fuerst, P. (1983). An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics, 103, 513–27.Google ScholarPubMed
Birky, C. W., Maruyama, T., and Fuerst, P. (1989). Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effect of heteroplasmic cells, and comparison to nuclear genes. Genetics, 121, 613–27.Google Scholar
Brynnel, E. U., Kurland, G. C., Moran, N. A., and Andersson, G. C. (1998). Evolutionary rates for tuf genes in endosymbionts of aphids. Mol Biol Evol, 15, 574–82.CrossRefGoogle ScholarPubMed
Buchner, P. (1965). Endosymbiosis of animals with plant microorganisms. New York: Interscience.Google Scholar
Crow, J. F., and Kimura, M. (1970). An introduction to population genetics theory. New York: Harper and Row.Google Scholar
Daubin, V., and Moran, N. A. (2004). Comment of the “Origins of genome complexity”. Science, 306, 978a.CrossRefGoogle Scholar
Degnan, P. H., Lazarus, A. B., Brock, C. D., and Wernegreen, J. J. (2004). Host-symbiont stability and fast evolutionary rates in an ant-bacterium association: cospeciation of Camponotus species and their endosymbionts, Candidatus Blochmannia. Syst Biol, 53, 95–110.CrossRefGoogle Scholar
Degnan, P. H., Lazarus, A. B., and Wernegreen, J. J. (2005). Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res, 15, 1023–33.CrossRefGoogle ScholarPubMed
Delmotte, F., Rispe, C., Schaber, J., Silva, F. J., and Moya, A. (2006). Tempo and mode of early gene loss in endosymbiotic bacteria from insects. BMC Evol Biol, 6, 56.CrossRefGoogle ScholarPubMed
Douglas, A.E. (1998). Nutritional interactions in insect-microbial symbiosis. Annu Rev Entomol, 43, 17–37.CrossRefGoogle Scholar
Funk, D. J., Wernegreen, J. J., and Moran, N. A. (2001). Intraspecific variation in symbiont genomes: bottlenecks and the aphid-Buchnera association. Genetics, 157, 477–89.Google ScholarPubMed
Gòmez-Valero, L., Latorre, A., and Silva, F. J. (2007). The evolutionary fate of nonfunctional DNA in the bacterial endosymbiont Buchnera aphidicola. Mol Biol Evol, 21, 2172–81.CrossRefGoogle Scholar
Itoh, T., Martin, W., and Nei, M. (2002). Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc Natl Acad Sci USA, 99, 12944–8.CrossRefGoogle ScholarPubMed
Kimura, M., and Ohta, M. (1969). The average number of generations until fixation of a mutant gene in a finite population. Genetics, 61, 763–71.Google Scholar
Komaki, K., and Ishikawa, H. (1999). Intracellular bacterial symbionts of aphids posses many genomic copies per bacterium. J Mol Evol, 48, 717–22.CrossRefGoogle Scholar
Komaki, K., and Ishikawa, H. (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, 253–8.CrossRefGoogle ScholarPubMed
Lynch, M. (2005). The origins of eukaryotic gene structure. Mol Biol Evol, 23, 450–68.CrossRefGoogle ScholarPubMed
Lynch, M. (2006). Streamlining and simplification of microbial genome architecture. Annu Rev Microbiol, 60, 327–49.CrossRefGoogle ScholarPubMed
Lynch, M., and Conery, J. S. (2003). The origins of genome complexity. Science, 302, 1401–4.CrossRefGoogle ScholarPubMed
Lynch, M., and Conery, J. S. (2004). Response to comment on “The origin of genome complexity”. Science, 306, 978b.CrossRefGoogle Scholar
Lynch, M., Koskella, B., and Schaack, S. (2006). Mutation pressure and the evolution of the organelle genomic architecture. Science, 311, 1727–30.CrossRefGoogle ScholarPubMed
Martínez-Torres, D., Simon, J. C., Fereres, A., and Moya, A. (1996). Genetic variation in natural populations of the aphid Rhopalosiphum padi as revealed by maternally inherited markers. Mol Ecol, 5, 659–70.CrossRefGoogle Scholar
Mira, A., and Moran, N. A. (2002). Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb Ecol, 44, 137–43.CrossRefGoogle ScholarPubMed
Moran, N. A. (1996). Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc Natl Acad Sci USA, 93, 2873–8.CrossRefGoogle ScholarPubMed
Munson, M. A., Baumann, P., and Kinsey, M. G. (1991). Buchnera gen. nov., and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. Int J Syst Bacteriol, 41, 566–8.CrossRefGoogle Scholar
Ochmann, H., Elwyn, S., and Moran, N. A. (1999). Calibrating bacterial evolution. Proc Natl Acad Sci USA, 96, 12638–43.CrossRefGoogle Scholar
Pérez-Brocal, V., Gil, R., Ramos, S., et al. (2006). A small microbial genome: the end of a long intimate relationship?Science, 314, 312–13.CrossRefGoogle Scholar
Rand, D. M., and Harrison, R. G. (1986). Mitochondrial DNA transmission genetics in crickets. Genetics, 114, 955–70.Google ScholarPubMed
Rispe, C., and Moran, N. A. (2000). Accumulation of deleterious mutations in endosymbionts: Muller's ratchet with two levels of selection. Am Naturalist, 156, 425–41.Google ScholarPubMed
Rispe, C., Delmotte, F., Ham, R. C. H. J., and Moya, A. (2004). Mutational and selective pressures on codon and amino acid usage in Buchnera, endosymbiotic bacteria of aphids. Genome Res, 14, 44–53.CrossRefGoogle ScholarPubMed
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, 1123–32.CrossRefGoogle ScholarPubMed
Ham, R. C. H. J., Kamerbeek, J., Palacios, C., et al. (2003). Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci USA, 100, 581–6.Google ScholarPubMed
Dohlen, C. D., and Moran, N. A. (2000). Mitochondrial ribosomal sequences and fossils support a rapid radiation of aphids in the Cretaceous and multiple origins of a complex life cycle. Biol J Linn Soc, 71, 689–717.CrossRefGoogle Scholar
Wilkinson, T. L., and Douglas, A. E. (1998). Host cell allometry and regulation of the symbiosis between pea aphids, Acyrthosiphon pisum, and bacteria, Buchnera. J Insect Physiol, 44, 629–35.CrossRefGoogle Scholar
Wright, S. (1969). Evolution and the genetics of populations, Vol. 2. Chicago: Chicago University Press.Google Scholar

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