Abstract
While most commonly associated with prokaryotes, horizontal gene transfer (HGT) can also have a significant influence on the evolution of microscopic eukaryotes. Systematic analysis of HGT in the genomes of the oomycetes, filamentous eukaryotic microorganisms in the Stramenopiles-Alveolates-Rhizaria (SAR) supergroup, has to date focused mainly on intradomain transfer events between oomycetes and fungi. Using systematic whole-genome analysis followed by phylogenetic reconstruction, we have investigated the extent of interdomain HGT between bacteria and plant-pathogenic oomycetes. We report five putative instances of HGT from bacteria into the oomycetes. Two transfers were found in Phytophthora species, including one unique to the cucurbit pathogen Phytophthora capsici. Two were found in Pythium species only, and the final transfer event was present in Phytopythium and Pythium species, the first reported bacterium-inherited genes in these genera. Our putative transfers included one protein that appears to be a member of the Pythium secretome, metabolic proteins, and enzymes that could potentially break down xenobiotics within the cell. Our findings complement both previous reports of bacterial genes in oomycete and SAR genomes and the growing body of evidence suggesting that interdomain transfer from prokaryotes into eukaryotes occurs more frequently than previously thought. IMPORTANCE Horizontal gene transfer (HGT) is the nonvertical inheritance of genetic material by transfer between different species. HGT is an important evolutionary mechanism for prokaryotes and in some cases is responsible for the spread of antibiotic resistance from resistant to benign species. Genome analysis has shown that examples of HGT are not as frequent in eukaryotes, but when they do occur they may have important evolutionary consequences. For example, the acquisition of fungal genes by an ancestral Phytophthora (plant destroyer) species is responsible for the large repertoire of enzymes in the plant-degrading arsenal of modern-day Phytophthora species. In this analysis, we set out to systematically search oomycete genomes for evidence of interdomain HGT (transfer of bacterial genes into oomycete species). Our results show that interdomain HGT is rare in oomycetes but has occurred. We located five well-supported examples, including one that could potentially break down xenobiotics within the cell.
Highlights
While most commonly associated with prokaryotes, horizontal gene transfer (HGT) can have a significant influence on the evolution of microscopic eukaryotes
Over 700 bacterial genes are present across fungi, with a particular concentration in Pezizomycotina [8]; 71 putative bacterial genes have been identified in Hydra vulgaris [9]; and the plant-parasitic nematode Meloidogyne incognita secretes cell wall-degrading enzymes inherited from soil-dwelling Actinomycetales and the betaproteobacterium Ralstonia solanacearum [10]
Filtering for redundancy, 64 unique candidate maximum-likelihood Horizontal gene transfer (HGT) phylogenies with 100 bootstrap replicates (Table 2) were generated using PhyML with the best-fit model for each phylogeny chosen by ProtTest [38]
Summary
While most commonly associated with prokaryotes, horizontal gene transfer (HGT) can have a significant influence on the evolution of microscopic eukaryotes. Our putative transfers included one protein that appears to be a member of the Pythium secretome, metabolic proteins, and enzymes that could potentially break down xenobiotics within the cell. Our findings complement both previous reports of bacterial genes in oomycete and SAR genomes and the growing body of evidence suggesting that interdomain transfer from prokaryotes into eukaryotes occurs more frequently than previously thought. The acquisition of fungal genes by an ancestral Phytophthora (plant destroyer) species is responsible for the large repertoire of enzymes in the plant-degrading arsenal of modern-day Phytophthora species In this analysis, we set out to systematically search oomycete genomes for evidence of interdomain HGT (transfer of bacterial genes into oomycete species). Over 700 bacterial genes are present across fungi, with a particular concentration in Pezizomycotina [8]; 71 putative bacterial genes have been identified in Hydra vulgaris [9]; and the plant-parasitic nematode Meloidogyne incognita secretes cell wall-degrading enzymes inherited from soil-dwelling Actinomycetales and the betaproteobacterium Ralstonia solanacearum [10]
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