Lateral gene transfer as a support for the tree of life

Abstract

Lateral gene transfer (LGT), the acquisition of genes from other species, is a major evolutionary force. However, its success as an adaptive process makes the reconstruction of the history of life an intricate puzzle: If no gene has remained unaffected during the course of life's evolution, how can one rely on molecular markers to reconstruct the relationships among species? Here, we take a completely different look at LGT and its impact for the reconstruction of the history of life. Rather than trying to remove the effect of LGT in phylogenies, and ignoring as a result most of the information of gene histories, we use an explicit phylogenetic model of gene transfer to reconcile gene histories with the tree of species. We studied 16 bacterial and archaeal phyla, representing a dataset of 12,000 gene families distributed in 336 genomes. Our results show that, in most phyla, LGT provides an abundant phylogenetic signal on the pattern of species diversification and that this signal is robust to the choice of gene families under study. We also find that LGT brings an abundant signal on the location of the root of species trees, which has been previously overlooked. Our results quantify the great variety of gene transfer rates among lineages of the tree of life and provide strong support for the "complexity hypothesis," which states that genes whose products participate to macromolecular protein complexes are relatively resistant to transfer. genome evolution | phylogeny | bacteria | archaea

Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

“…Using simulations, we show that our method is robust to realistic levels of reconstruction errors and sources of systematic bias. Examining a diverse set of prokaryotic phyla, we find that the topology of the reconstructed species tree is very similar to results obtained with classic phylogenomics methods, consistent with the observation (13,19,27) that concatenate and supertree approaches are able to extract a robust signal even in the presence of substantial LGT. However, aggregate approaches may be sensitive to biased LGT (12), a caveat which is especially relevant in light of recent empirical evidence of strong habitat drivers in LGT (28).…”

“…We then inferred the chronologically ordered phylogenies for 10 prokaryotic phyla from the dataset in ref. 19. Comparing the reconstructed species tree topologies to unrooted trees obtained by established methods (Table 1), we find that our results are generally very similar to phylogenomics methods that rely on single copy genes but differ more markedly from 16S rRNA phylogenies.…”

“…Table 1, we extracted all families with trees from version 4 of the HOGENOM database (20) for 10 prokaryotic phyla using the species selection of ref. 19. We retained all families with at least two genes in the set of species considered.…”

“…), and the consensus tree ML trees of universal families (Cs.). † "Same" indicates a root on the same bipartition as (19), "near" and "far" indicate neighboring or more distant bipartition, and "other" that the root bipartition in (19) was not present. Using maximum likelihood reconciliations averaged over gene tree roots and origination positions, we also estimated the number of genes in ancestral genomes of cyanobacteria (Fig.…”

Integrative modeling of gene and genome evolution roots the archaeal tree of life

“…The use of gene duplications to root major clades has a venerable history in molecular evolution (45), particularly for resolving the root of the tree of life (11)(12)(13)(62)(63)(64). More recently, it has been appreciated that gene gains, losses, and horizontal transfers also contain information about the root of a species tree that can be integrated using probabilistic gene tree-species tree reconciliation approaches (65)(66)(67). We used a recently developed method known as amalgamated likelihood estimation (ALE) (67) to calculate gene family likelihoods for each of the 31,236 homologous gene families encoded by our sample of 62 archaeal genomes, under a set of candidate root positions on the archaeal species tree ( Fig.…”