Recent events dominate interdomain lateral gene transfers between prokaryotes and eukaryotes and, with the exception of endosymbiotic gene transfers, few ancient transfer events persist - PubMed (original) (raw)

Recent events dominate interdomain lateral gene transfers between prokaryotes and eukaryotes and, with the exception of endosymbiotic gene transfers, few ancient transfer events persist

Laura A Katz. Philos Trans R Soc Lond B Biol Sci. 2015.

Abstract

While there is compelling evidence for the impact of endosymbiotic gene transfer (EGT; transfer from either mitochondrion or chloroplast to the nucleus) on genome evolution in eukaryotes, the role of interdomain transfer from bacteria and/or archaea (i.e. prokaryotes) is less clear. Lateral gene transfers (LGTs) have been argued to be potential sources of phylogenetic information, particularly for reconstructing deep nodes that are difficult to recover with traditional phylogenetic methods. We sought to identify interdomain LGTs by using a phylogenomic pipeline that generated 13 465 single gene trees and included up to 487 eukaryotes, 303 bacteria and 118 archaea. Our goals include searching for LGTs that unite major eukaryotic clades, and describing the relative contributions of LGT and EGT across the eukaryotic tree of life. Given the difficulties in interpreting single gene trees that aim to capture the approximately 1.8 billion years of eukaryotic evolution, we focus on presence-absence data to identify interdomain transfer events. Specifically, we identify 1138 genes found only in prokaryotes and representatives of three or fewer major clades of eukaryotes (e.g. Amoebozoa, Archaeplastida, Excavata, Opisthokonta, SAR and orphan lineages). The majority of these genes have phylogenetic patterns that are consistent with recent interdomain LGTs and, with the notable exception of EGTs involving photosynthetic eukaryotes, we detect few ancient interdomain LGTs. These analyses suggest that LGTs have probably occurred throughout the history of eukaryotes, but that ancient events are not maintained unless they are associated with endosymbiotic gene transfer among photosynthetic lineages.

Keywords: endosymbiotic gene transfer; eukaryotic tree of life; horizontal gene transfer; phylogenomics.

© 2015 The Author(s).

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Figures

Figure 1.

Figure 1.

An example of a recent interdomain LGT from prokaryotes to one minor clade (Metazoa) in one major clade (Opisthokonta) of eukaryotes. This tree exemplifies the many recent (e.g. 1MC1mc) interdomain transfers detected in this study (table 2 and figure 3). Abbreviations of taxa are as in table 1 and electronic supplementary material, S1, and the number following each name is a unique identifier from either OrthoMCL or GenBank. Analyses of this gene used PROTGAMMA, the best-fitting LG model and default parameters as implemented in R

ax

ML [49,50]. Most nodes are poorly supported and only bootstrap values above 80% are shown. Monophyletic clades are marked with solid lines, whereas the complex relationships among prokaryotes in the dashed clades probably represent a combination of poorly resolved phylogeny, LGT among prokaryotes and gene loss.

Figure 2.

Figure 2.

Recent LGT events mapped onto representative lineages from the eukaryotic tree of life. Numbers at nodes represent the LGT events in table 3, and the synthetic tree is arbitrarily rooted on Opisthokonta. Numbers marked by asterisk are found in at least three minor clades within major clades and may represent synapomorphies for major clades. Arrows on the right mark shared putative LGTs found between non-sister minor clades. Numbers in green (grey) in parentheses are genes where eukaryotes fall sister to cyanobacteria and are hence putative EGTs. For simplicity, only a subset of lineages are included here and full taxonomic distributions can be found in the electronic supplementary material, tables S1 and S2. (Online version in colour.)

Figure 3.

Figure 3.

Significant networks among lineages as determined by COPAP [54] based on presence–absence of LGTs. The green (dark) taxa are predominantly photosynthetic, and networks involving these minor clades indicate the potential influence of EGT on photosynthetic lineages. There is also a significant relationship between Entamoeba spp. (Am_ar) and parabasalids (Ex_pa) as has been previously observed [,–57]. The linking of fungi (Op_fu) and microbial opisthokonts (Op_ot; other Opisthokonta = Ichthyosporea plus lineages that are incertae sedis) probably represents shared retention of LGT events. (Online vesion in colour.)

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