The balance of driving forces during genome evolution in prokaryotes

Abstract

Genomes are shaped by evolutionary processes such as gene genesis, horizontal gene transfer (HGT), and gene loss. To quantify the relative contributions of these processes, we analyze the distribution of 12,762 protein families on a phylogenetic tree, derived from entire genomes of 41 Bacteria and 10 Archaea. We show that gene loss is the most important factor in shaping genome content, being up to three times more frequent than HGT, followed by gene genesis, which may contribute up to twice as many genes as HGT. We suggest that gene gain and gene loss in prokaryotes are balanced; thus, on average, prokaryotic genome size is kept constant. Despite the importance of HGT, our results indicate that the majority of protein families have only been transmitted by vertical inheritance. To test our method, we present a study of strain-specific genes of Helicobacter pylori, and demonstrate correct predictions of gene loss and HGT for at least 81% of validated cases. This approach indicates that it is possible to trace genome content history and quantify the factors that shape contemporary prokaryotic genomes.

Figure 1

Comparison of observed and expected ratio of gene loss over HGT at various HGT penalties. The expected ratio implied by the model is shown in black (diamonds), and observed results are represented in blue (squares) for the 16S rRNA tree, green (circles) for the gene content tree, and gray (triangles) for the shuffled tree. The genuine trees are in agreement with the model (intersecting the expected linear curve) at HGT penalty values between 2 and 3. The shuffled tree overpredicts HGT at any tested HGT penalty value.

Figure 2

The difference between gene gain and loss at various HGT penalties. The results for 16S rRNA, gene content, and shuffled trees are shown; represented as in Figure 1. The concordance of the two genuine (16S rRNA and gene content) trees is evident, contrasted to the shuffled tree. Genome stability (signified by zero difference, bold horizontal line) is achieved with HGT penalty values between 2 and 3.

Figure 3

The fraction of families predicted to be involved in horizontal gene transfer at different HGT penalties. Percentages for the 16S rRNA tree are represented by blue bars, for the gene content tree by green bars, and for the shuffled tree by grey bars.

Figure 4

A segment of the 16S rRNA tree, with the predicted number for protein families at each node displayed (green), and the number of families gained (red) or lost (blue) for each branch. The genomes represented in this tree segment are: Campylobacter jejuni (CJEJ), Helicobacter pylori strains 26695 (HPYL-2) and J99 (HPYL-J), Mesorhizobium loti (MLOT), Caulobacter crescentus (CCRE), Rickettsia prowazekii (RPRO), Xyllela fastidiosa (XFAS), and Neisseria meningitidis strains Z2491 (NMEN-Z) and MC58 (NMEN-M). See text for discussion.