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, 10 (4), R36

The Transferome of Metabolic Genes Explored: Analysis of the Horizontal Transfer of Enzyme Encoding Genes in Unicellular Eukaryotes

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The Transferome of Metabolic Genes Explored: Analysis of the Horizontal Transfer of Enzyme Encoding Genes in Unicellular Eukaryotes

John W Whitaker et al. Genome Biol.

Abstract

Background: Metabolic networks are responsible for many essential cellular processes, and exhibit a high level of evolutionary conservation from bacteria to eukaryotes. If genes encoding metabolic enzymes are horizontally transferred and are advantageous, they are likely to become fixed. Horizontal gene transfer (HGT) has played a key role in prokaryotic evolution and its importance in eukaryotes is increasingly evident. High levels of endosymbiotic gene transfer (EGT) accompanied the establishment of plastids and mitochondria, and more recent events have allowed further acquisition of bacterial genes. Here, we present the first comprehensive multi-species analysis of E/HGT of genes encoding metabolic enzymes from bacteria to unicellular eukaryotes.

Results: The phylogenetic trees of 2,257 metabolic enzymes were used to make E/HGT assertions in ten groups of unicellular eukaryotes, revealing the sources and metabolic processes of the transferred genes. Analyses revealed a preference for enzymes encoded by genes gained through horizontal and endosymbiotic transfers to be connected in the metabolic network. Enrichment in particular functional classes was particularly revealing: alongside plastid related processes and carbohydrate metabolism, this highlighted a number of pathways in eukaryotic parasites that are rich in enzymes encoded by transferred genes, and potentially key to pathogenicity. The plant parasites Phytophthora were discovered to have a potential pathway for lipopolysaccharide biosynthesis of E/HGT origin not seen before in eukaryotes outside the Plantae.

Conclusions: The number of enzymes encoded by genes gained through E/HGT has been established, providing insight into functional gain during the evolution of unicellular eukaryotes. In eukaryotic parasites, genes encoding enzymes that have been gained through horizontal transfer may be attractive drug targets if they are part of processes not present in the host, or are significantly diverged from equivalent host enzymes.

Figures

Figure 1
Figure 1
The predicted extent of the transfer of genes encoding metabolic enzymes. The bar chart shows the total number of enzymes that were identified as being present (high-confidence; see text) in each organism group. The numbers of enzymes whose genes were predicted as originating from EGT and HGT are indicated with green and blue, respectively.
Figure 2
Figure 2
Xylose degradation in Leishmania. The figure shows a possible xylose degradation pathway in Leishmania. Enzymes shown in black are predicted as being present, the genes for enzymes shown in blue are predicted as being present and as being HGTs and the enzymes shown in grey are not predicted as being present. PRPP, 5-Phospho-alpha-D-ribose 1-diphosphate.
Figure 3
Figure 3
Lipopolysaccharide biosynthesis in Phytophthora. Enzymes that carry out reactions are labeled by E. coli gene name. The genes of the enzymes colored blue were predicted as being HGTs and the genes of the enzymes colored green were predicted as being EGTs. Enzymes colored black were predicted as being present in both Phytophthora genomes with profile E-values ≤ 10-10. Enzymes in grey were predicted as being present in at least one Phytophthora genome with E-values 10-1 ≥ E > 10-10.

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