Deletional bias and the evolution of bacterial genomes

doi:10.1016/S0168-9525(01)02447-7

Trends in Genetics

Volume 17, Issue 10, 1 October 2001, Pages 589-596

https://doi.org/10.1016/S0168-9525(01)02447-7 Get rights and content

Abstract

Although bacteria increase their DNA content through horizontal transfer and gene duplication, their genomes remain small and, in particular, lack nonfunctional sequences. This pattern is most readily explained by a pervasive bias towards higher numbers of deletions than insertions. When selection is not strong enough to maintain them, genes are lost in large deletions or inactivated and subsequently eroded. Gene inactivation and loss are particularly apparent in obligate parasites and symbionts, in which dramatic reductions in genome size can result not from selection to lose DNA, but from decreased selection to maintain gene functionality. Here we discuss the evidence showing that deletional bias is a major force that shapes bacterial genomes.

Section snippets

Deletional bias in bacterial genomes

Although duplications and resulting paralogous genes are apparent in many bacterial genomes ¹², there is growing evidence that the primary route through which bacterial species obtain new genes is by lateral transfer 15, 16, 17. If lateral gene transfer is an ongoing process, why are bacterial genomes compact and not ever-expanding because of the influx of foreign sequences? The obvious answer is that lineages must undergo the inactivation and loss of genes, and the elimination of the

Degraded genes and persistent pseudogenes

The overall proportion of noncoding DNA is fairly similar (around 12%) among the fully sequenced genomes of different taxonomic groups (Fig. 3). These noncoding sequences provide a glimpse of the effects of deletional bias. For example, the large number of gene regions conserved between Buchnera and E. coli allows a direct assessment of how the extreme reduction of genomes occurs ²⁹. Within regions that show synteny with E. coli, spacers from Buchnera can be divided into two categories:

A model for genome size evolution in bacteria

These observations, from analyses of complete genomic sequences, suggest a simple model for the evolution of bacterial genome size based on the outcome of several opposing forces (Fig. 4). Deletional bias and genetic drift cause genomes to contract, whereas selection on gene function causes genomes to maintain DNA. Accretions in genome size depend on either duplications or the acquisition of exogenous DNA, but these events are only effective if the new genes confer some benefit (or if the DNA

Acknowledgements

We thank Jacob Russell, Alex Kondrashov and two anonymous reviewers for helpful comments. The work was supported by grants GM55535 and GM56120 from NIH and grant DEB-9978518 from NSF.

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Trends in Genetics

ReviewDeletional bias and the evolution of bacterial genomes

Abstract

Section snippets

Deletional bias in bacterial genomes

Degraded genes and persistent pseudogenes

A model for genome size evolution in bacteria

Acknowledgements

Annu. Rev. Genet.

Chromosoma

Trends Microbiol.

The modulation of DNA content: proximate causes and ultimate consequences

Genome Res.

The minimal gene complement of Mycoplasma genitalium

Science

Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti

DNA Res.

Life with 6000 genes

Science

A physical map of the human genome

Nature

The sequence of the human genome

Science

Evolution of the bacterial genome

Annu. Rev. Microbiol.

Measuring genome evolution

Proc. Natl. Acad. Sci. U. S. A.

Lineage-specific gene expansions in bacterial and archaeal genomes

Genome Res.

Heterogeneity of genome sizes among natural isolates of Escherichia coli

J. Bacteriol.

Lateral gene transfer and the nature of bacterial innovation

Nature

Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima

Nature

Molecular archaeology of the Escherichia coli genome

Proc. Natl. Acad. Sci. U. S. A.

Patterns of nucleotide substitution in pseudogenes and functional genes

J. Mol. Evol.

Review
Deletional bias and the evolution of bacterial genomes