A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer

Abstract

Background: Lateral 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.

Results: Here 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.

Conclusion: Determining 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.

Figure 1

Bayesian phylogenetic tree of ribulose-5-phosphate-3 epimerase (RPE). The tree was inferred from 183 amino acid characters with branch lengths estimated using PROML. Bootstrap values > 50% are shown. Values shown above a node correspond to PHYML bootstrap support, those below a node correspond to WEIGHBOR support. Eukaryotic sequences are enclosed in boxes where blue corresponds to the major clade of cytosolic proteins, green corresponds to plastid-targeted proteins, and red corresponds to bacterium-derived genes. Filled circles adjacent to taxon names indicate that a complete genome is available from this organism.

Figure 3

Bayesian phylogenetic tree of transketolase (TK). The tree was inferred from 473 amino acid characters with branch lengths estimated using PROML. Bootstrap values > 50% are shown. Values shown above a node correspond to PHYML bootstrap support, those below a node correspond to WEIGHBOR support. Eukaryotic sequences are enclosed in boxes where blue corresponds to the major clade of cytosolic proteins, green corresponds to plastid-targeted proteins, and red corresponds to bacterium-derived genes. Filled circles adjacent to taxon names indicate that a complete genome is available from this organism. Multiple isoforms of TK are present in the diatom genomes, both a Chlamydia type TK as well as a eukaryotic form of this enzyme are present. Two types of TK are present in Euglena as well, a form related to the plastid TK of other eukaryotes as well as a Chlamydia type.

Figure 4

Transketolase alignment flanking a 4-amino acid insertion present in diatom, dinoflagellate and chlorarachniophyte TK-Ch genes. A nearby 11- to 15-amino acid insertion characterizes a mixed group of CFB bacteria and proteobacteria as well as the amoebozoan Hartmannella vermiformis and the dinoflagellate Karlodinium micrum. Eukaryotic TKs putatively derived from lateral transfer events are surrounded by black squares (TK-Ch being the lower box).

Figure 2

Bayesian phylogenetic tree of glyceraldehyde-3-phosphate dehydrogenase (GAPDH). The tree was inferred from 278 amino acid characters with branch lengths estimated using PROML. Bootstrap values > 50% are shown. Values shown above a node correspond to PHYML bootstrap support, those below a node correspond to WEIGHBOR support. Eukaryotic sequences are enclosed in boxes where blue corresponds to the major clade of cytosolic proteins, green corresponds to plastid-targeted proteins, and red corresponds to bacterium-derived genes (the B. natans plastid targeted GAPDH is also bacterium-derived and is coloured red). Filled circles adjacent to taxon names indicate that a complete genome is available for this organism.