Evolution of gene order conservation in prokaryotes

Abstract

Background: As more complete genomes are sequenced, conservation of gene order between different organisms is emerging as an informative property of the genomes. Conservation of gene order has been used for predicting function and functional interactions of proteins, as well as for studying the evolutionary relationships between genomes. The reasons for the maintenance of gene order are still not well understood, as the organization of the prokaryote genome into operons and lateral gene transfer cannot possibly account for all the instances of conservation found. Comprehensive studies of gene order are one way of elucidating the nature of these maintaining forces.

Results: Gene order is extensively conserved between closely related species, but rapidly becomes less conserved among more distantly related organisms, probably in a cooperative fashion. This trend could be universal in prokaryotic genomes, as archaeal genomes are likely to behave similarly to bacterial genomes. Gene order conservation could therefore be used as a valid phylogenetic measure to study relationships between species. Even between very distant species, remnants of gene order conservation exist in the form of highly conserved clusters of genes. This suggests the existence of selective processes that maintain the organization of these regions. Because the clusters often span more than one operon, common regulation probably cannot be invoked as the cause of the maintenance of gene order.

Conclusions: Gene order conservation is a genomic measure that can be useful for studying relationships between prokaryotes and the evolutionary forces shaping their genomes. Gene organization is extensively conserved in some genomic regions, and further studies are needed to elucidate the reason for this conservation.

Figure 1

Conservation of gene order in prokaryotic genomes in relation to phylogenetic distance, measured as the number of substitutions in SSU rRNA. Each point represents a pair of species. (a) Results for all species. (b) Same plot as in (a), but with Archaea removed and values for some bacterial species highlighted.

Figure 2

Conservation of gene order between all prokaryotic species in relation to phylogenetic distance, estimated by means of phylogenies of universal conserved proteins. Each point represents a pair of species.

Figure 3

Conservation of gene order in relation to common gene content within and between prokaryotic domains. Each point represents a pair of species. (a) Results for all species. (b) Same plot as in (a), but with Archaea removed and values for some bacterial species highlighted.

Figure 4

Gene order conservation in the species studied, using (a) Escherichia coli and (b) Xylella fastidiosa as a reference. Position in the reference genome means number of genes from minute zero. Individual species are plotted in the y axis and are ordered according to their phylogenetic distance (estimated by SSU rRNA substitutions) to the reference species. The more closely related species are shown lower down and more distantly related species higher up the axis. Species names are listed in Table 2. Blue dots indicate genes belonging to conserved runs for each species. A horizontal green line separates Bacteria from Archaea. (a) For E. coli, yellow lines show the regions with especially high conservation of gene order. A detailed study of these regions can be found in Table 1. The origin and terminus of replication are marked O and T, respectively, at the bottom of the graph. (b) For X. fastidiosa, red lines indicate regions of high frequency of unique genes [25]. A low degree of gene order conservation was found in these regions.

Table 1

^*Location of the gene in the genome, expressed in absolute number of genes from minute zero. ^†Percentage of conservation of gene order with respect to other genomes, expressed as the ratio between the number of times that the gene is conserved in the run and the total number of times that the gene is present. ^‡The functional class is a general assignment of function as provided by the EUCLID system. Arrows in the right part of the figure indicate operons. Red tips in the arrows indicate that the operon continues in that direction, therefore containing genes not included in the run. Only operons for which experimental evidence is available are considered.