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Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths.

Kloesges T, Popa O, Martin W, Dagan T - Mol. Biol. Evol. (2010)

Bottom Line: The network of shared proteins reveals modularity structure that does not correspond to current classification schemes.Using a minimal lateral network approach, we compared LGT rates at different phylogenetic depths.Hence, our results indicate that the rate of gene acquisition per protein family is similar at the level of species (by recombination) and at the level of classes (by LGT).

View Article: PubMed Central - PubMed

Affiliation: Institute of Botany III, Heinrich-Heine University Düsseldorf, Düsseldorf, Germany.

ABSTRACT
Lateral gene transfer (LGT) is an important mechanism of natural variation among prokaryotes. Over the full course of evolution, most or all of the genes resident in a given prokaryotic genome have been affected by LGT, yet the frequency of LGT can vary greatly across genes and across prokaryotic groups. The proteobacteria are among the most diverse of prokaryotic taxa. The prevalence of LGT in their genome evolution calls for the application of network-based methods instead of tree-based methods to investigate the relationships among these species. Here, we report networks that capture both vertical and horizontal components of evolutionary history among 1,207,272 proteins distributed across 329 sequenced proteobacterial genomes. The network of shared proteins reveals modularity structure that does not correspond to current classification schemes. On the basis of shared protein-coding genes, the five classes of proteobacteria fall into two main modules, one including the alpha-, delta-, and epsilonproteobacteria and the other including beta- and gammaproteobacteria. The first module is stable over different protein identity thresholds. The second shows more plasticity with regard to the sequence conservation of proteins sampled, with the gammaproteobacteria showing the most chameleon-like evolutionary characteristics within the present sample. Using a minimal lateral network approach, we compared LGT rates at different phylogenetic depths. In general, gene evolution by LGT within proteobacteria is very common. At least one LGT event was inferred to have occurred in at least 75% of the protein families. The average LGT rate at the species and class depth is about one LGT event per protein family, the rate doubling at the phylum level to an average of two LGT events per protein family. Hence, our results indicate that the rate of gene acquisition per protein family is similar at the level of species (by recombination) and at the level of classes (by LGT). The frequency of LGT per genome strongly depends on the species lifestyle, with endosymbionts showing far lower LGT frequencies than free-living species. Moreover, the nature of the transferred genes suggests that gene transfer in proteobacteria is frequently mediated by conjugation.

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A minimal LGT network for proteobacterial classes alpha (A), beta (B), and gamma (C). Vertical edges are indicated in gray, with both the width and the shading of the edge shown proportional to the number of inferred vertically inherited genes along the edge (see scale bar). The lateral network is indicated by edges that do not map onto the vertical component, with number of genes per edge indicated in color (see scale bar). The MLN showing only edges of weight ≥5 genes.
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fig6: A minimal LGT network for proteobacterial classes alpha (A), beta (B), and gamma (C). Vertical edges are indicated in gray, with both the width and the shading of the edge shown proportional to the number of inferred vertically inherited genes along the edge (see scale bar). The lateral network is indicated by edges that do not map onto the vertical component, with number of genes per edge indicated in color (see scale bar). The MLN showing only edges of weight ≥5 genes.

Mentions: The connectivity distribution in the alphaproteobacterial MLN is bimodal, suggesting two groups of species that are either weakly or strongly connected within the lateral network (fig. 5B). The graphical representation of the MLN for that class reveals that the Rickettsiales comprise the weakly connected group (fig. 6A). In our data set, the order Rickettsiales includes 21 endosymbiotic parasites from the genera Anaplasma, Ehrlichia, and Rickettsia. The host-associated lifestyle of these species is a barrier to LGT in many cases and probably the reason for their low connectivity in the MLN. The connectivity distribution in the betaproteobacterial MLN is almost uniform (fig. 5C) with similar frequencies of nodes across the connectivity range (0–50 edges per node) and five more nodes whose connectivity is above this range. Clades of symbionts within the betaproteobacterial MLN, the Neisseriales and Nitrodomonadales, are weakly connected (fig. 6B). The Burkholderiales in our sample include 31 species of diverse lifestyles that account for the majority (60%) of betaproteobacterial species in the data. The overall gene distribution patterns are quite uniform across that order (fig. 1), yet the parasites among them (Ralstonia species) having lower connectivity than the free-living species (Burkholderia species; fig. 6B).


Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths.

Kloesges T, Popa O, Martin W, Dagan T - Mol. Biol. Evol. (2010)

A minimal LGT network for proteobacterial classes alpha (A), beta (B), and gamma (C). Vertical edges are indicated in gray, with both the width and the shading of the edge shown proportional to the number of inferred vertically inherited genes along the edge (see scale bar). The lateral network is indicated by edges that do not map onto the vertical component, with number of genes per edge indicated in color (see scale bar). The MLN showing only edges of weight ≥5 genes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3021791&req=5

fig6: A minimal LGT network for proteobacterial classes alpha (A), beta (B), and gamma (C). Vertical edges are indicated in gray, with both the width and the shading of the edge shown proportional to the number of inferred vertically inherited genes along the edge (see scale bar). The lateral network is indicated by edges that do not map onto the vertical component, with number of genes per edge indicated in color (see scale bar). The MLN showing only edges of weight ≥5 genes.
Mentions: The connectivity distribution in the alphaproteobacterial MLN is bimodal, suggesting two groups of species that are either weakly or strongly connected within the lateral network (fig. 5B). The graphical representation of the MLN for that class reveals that the Rickettsiales comprise the weakly connected group (fig. 6A). In our data set, the order Rickettsiales includes 21 endosymbiotic parasites from the genera Anaplasma, Ehrlichia, and Rickettsia. The host-associated lifestyle of these species is a barrier to LGT in many cases and probably the reason for their low connectivity in the MLN. The connectivity distribution in the betaproteobacterial MLN is almost uniform (fig. 5C) with similar frequencies of nodes across the connectivity range (0–50 edges per node) and five more nodes whose connectivity is above this range. Clades of symbionts within the betaproteobacterial MLN, the Neisseriales and Nitrodomonadales, are weakly connected (fig. 6B). The Burkholderiales in our sample include 31 species of diverse lifestyles that account for the majority (60%) of betaproteobacterial species in the data. The overall gene distribution patterns are quite uniform across that order (fig. 1), yet the parasites among them (Ralstonia species) having lower connectivity than the free-living species (Burkholderia species; fig. 6B).

Bottom Line: The network of shared proteins reveals modularity structure that does not correspond to current classification schemes.Using a minimal lateral network approach, we compared LGT rates at different phylogenetic depths.Hence, our results indicate that the rate of gene acquisition per protein family is similar at the level of species (by recombination) and at the level of classes (by LGT).

View Article: PubMed Central - PubMed

Affiliation: Institute of Botany III, Heinrich-Heine University Düsseldorf, Düsseldorf, Germany.

ABSTRACT
Lateral gene transfer (LGT) is an important mechanism of natural variation among prokaryotes. Over the full course of evolution, most or all of the genes resident in a given prokaryotic genome have been affected by LGT, yet the frequency of LGT can vary greatly across genes and across prokaryotic groups. The proteobacteria are among the most diverse of prokaryotic taxa. The prevalence of LGT in their genome evolution calls for the application of network-based methods instead of tree-based methods to investigate the relationships among these species. Here, we report networks that capture both vertical and horizontal components of evolutionary history among 1,207,272 proteins distributed across 329 sequenced proteobacterial genomes. The network of shared proteins reveals modularity structure that does not correspond to current classification schemes. On the basis of shared protein-coding genes, the five classes of proteobacteria fall into two main modules, one including the alpha-, delta-, and epsilonproteobacteria and the other including beta- and gammaproteobacteria. The first module is stable over different protein identity thresholds. The second shows more plasticity with regard to the sequence conservation of proteins sampled, with the gammaproteobacteria showing the most chameleon-like evolutionary characteristics within the present sample. Using a minimal lateral network approach, we compared LGT rates at different phylogenetic depths. In general, gene evolution by LGT within proteobacteria is very common. At least one LGT event was inferred to have occurred in at least 75% of the protein families. The average LGT rate at the species and class depth is about one LGT event per protein family, the rate doubling at the phylum level to an average of two LGT events per protein family. Hence, our results indicate that the rate of gene acquisition per protein family is similar at the level of species (by recombination) and at the level of classes (by LGT). The frequency of LGT per genome strongly depends on the species lifestyle, with endosymbionts showing far lower LGT frequencies than free-living species. Moreover, the nature of the transferred genes suggests that gene transfer in proteobacteria is frequently mediated by conjugation.

Show MeSH
Related in: MedlinePlus