Review
Microbial genome evolution: sources of variability

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Abstract

Comparative genome analyses of close relatives have yielded exciting insight into the sources of microbial genome variability with respect to gene content, gene order and evolution of genes with unknown functions. The genomes of free-living bacteria often carry phages and repetitive sequences that mediate genomic rearrangements in contrast to the small genomes of obligate host-associated bacteria. This suggests that genomic stability correlates with the genomic content of repeated sequences and movable genetic elements, and thereby with bacterial lifestyle. Genes with unknown functions present in a single species tend to be shorter than conserved, functional genes, indicating that the fraction of unique genes in microbial genomes has been overestimated.

Introduction

Differences in growth strategies and life histories of bacteria have left ‘footprints’ in the content and architecture of their genomes 1., 2•.. Over the past few years, an increasing number of closely related microbial genomes has been sequenced and compared 3••., 4••., 5., 6., 7., 8., 9., 10.. They are sufficiently similar to permit complete genome alignments, but divergent enough to allow estimates of the frequencies of mutations influencing their genomic structures 11., 12.. By quantifying these differences, we are now able to address questions related to the content and structure of microbial genomes. Can we identify common features in genomic architecture across bacterial taxa? How do genomes achieve functional flexibility? How does the ecology of a given species influence the stability of its genome?

In this review, we address some of these questions using a comparative genomics approach. First, we examine the stability of microbial genomes. Second, we analyse factors that influence the extent of genome variability, and last, we discuss possible explanations for the surprisingly high fraction of species-specific genes with unknown functions. Given the wide spectrum of taxa and lifestyles of species for which two or more complete genomes are available, we can now begin to relate genomic features to the ecology of the species.

Section snippets

Bacterial genome architecture

Gene position plots (dot plots) between bacterial genome pairs display the arrangement of genes in closely related genomes in a simple graphical format. Visual inspection of gene-position plots for bacteria with different lifestyles reveals a remarkable variation in genomic stability (Fig. 1). This provides a starting point for an analysis of the mutational and selective forces underlying the observed variability.

The most stable microbial genomes identified so far are those of aphid

Symmetric genome rearrangements

Manual inspections of the borders of rearrangements in Chlamydia spp. have shown that these are often symmetrically organised around the origin and terminus of replication [17••]. This pattern, illustrated in Fig. 1 with Chlamydia, Rickettsia and Salmonella, is thought to be the outcome of high recombination frequencies at the open replication forks 17••., 18.. Symmetric translocation and inversion events have also been identified in several other genomes, such as those of Helicobacter and

Single-gene translocations and insertion sequence elements

Insertion sequence (IS) elements may be particularly important as mediators of gene rearrangements by offering multiple similar sequences among which recombination can be initiated [22]. The Sulfolobus genomes have atypically high contents of IS elements. For example, as many as 170 IS elements have been identified in Sulfolobus solfataricus [23]. Thus, it may be no coincidence that single gene translocations have been particularly common in the genomes of Sulfolobus spp., as shown by the

Insertion–deletions and rearrangements

Bacterial genomes can achieve functional flexibility by differential gene expression 28., 29. and by variation in gene content [30], achieved by horizontal transfer [31•] or gene duplication [32•]. It is reasonable to assume that the degree of homology between a related genome pair is reciprocally related to the frequency of gene deletions and insertions in each of the lineages [30]. Surprisingly, the relative frequencies of insertions-deletions versus translocations-inversions are well

The mysterious orphans: are they real genes?

The fraction of genes with no homology to previously sequenced genes in other genera (so-called orphan genes) is normally about 25–30%. Because these orphans may represent genes that underlie the functional and metabolic diversity of a given species or its host specificity [40••], they are the primary targets for postgenomic experimental analyses. It is therefore of particular interest to understand the origin and evolution of the many unknown genes identified in the genome projects.

The genome

Conclusions

Comparative genomics has shown that bacterial genomes are highly variable, both structurally and functionally, and that the degree of genome flexibility is dependent on the content of repeated and mobile sequences such as IS elements, plasmids and phages. On one extreme, obligate intracellular symbionts have the smallest genomes and show the highest degree of stability, with a complete absence of genome rearrangements and gene innovation [3••]. At the other extreme, free-living species undergo

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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