Abstract
BackgroundLateral gene transfer is increasingly invoked to explain phylogenetic results that conflict with our understanding of organismal relationships. In eukaryotes, the most common observation interpreted in this way is the appearance of a bacterial gene (one that is not clearly derived from the mitochondrion or plastid) in a eukaryotic nuclear genome. Ideally such an observation would involve a single eukaryote or a small group of related eukaryotes encoding a gene from a specific bacterial lineage.ResultsHere we show that several apparently simple cases of lateral transfer are actually more complex than they originally appeared: in these instances we find that two or more distantly related eukaryotic groups share the same bacterial gene, resulting in a punctate distribution. Specifically, we describe phylogenies of three core carbon metabolic enzymes: transketolase, glyceraldehyde-3-phosphate dehydrogenase and ribulose-5-phosphate-3-epimerase. Phylogenetic trees of each of these enzymes includes a strongly-supported clade consisting of several eukaryotes that are distantly related at the organismal level, but whose enzymes are apparently all derived from the same lateral transfer. With less sampling any one of these examples would appear to be a simple case of bacterium-to-eukaryote lateral transfer; taken together, their evolutionary histories cannot be so simple. The distributions of these genes may represent ancient paralogy events or genes that have been transferred from bacteria to an ancient ancestor of the eukaryotes that retain them. They may alternatively have been transferred laterally from a bacterium to a single eukaryotic lineage and subsequently transferred between distantly related eukaryotes.ConclusionDetermining how complex the distribution of a transferred gene is depends on the sampling available. These results show that seemingly simple cases may be revealed to be more complex with greater sampling, suggesting many bacterial genes found in eukaryotic genomes may have a punctate distribution.
Highlights
Lateral gene transfer is increasingly invoked to explain phylogenetic results that conflict with our understanding of organismal relationships
It has been shown that the plastid-targeted ribulose-5-phosphate-3 epimerase (RPE) of the chlorarachniophyte B. natans is not related to other plastid-targeted or even cyanobacterial genes, as one would expect, but is instead closely related to the γ-proteobacterial genus Pseudomonas [15]
Phylogenetic analysis confirmed that RPE genes from the haptophytes Emiliania huxleyi, Prymnesium parvum and Pavlova lutheri are all of the γ-proteobacterial type, as are those from the diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum (Figure 1)
Summary
Lateral gene transfer is increasingly invoked to explain phylogenetic results that conflict with our understanding of organismal relationships. The most common observation interpreted in this way is the appearance of a bacterial gene (one that is not clearly derived from the mitochondrion or plastid) in a eukaryotic nuclear genome. Such an observation would involve a single eukaryote or a small group of related eukaryotes encoding a gene from a specific bacterial lineage. Convincing examples of prokaryote-to-eukaryote gene transfers have been described [13,14,15,16,17], and transfers between eukaryotes are known [15,18,19,20,21] While these studies make it clear that lateral transfer has affected eukaryotic nuclear genomes, the frequency of such events and the extent of their evolutionary impact, for eukaryote-toeukaryote lateral transfers remains unknown. Most known cases involve genes moving from a prokaryote to eukaryotes, whereas comparatively little is known about transfers between eukaryotes
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