The net of life: reconstructing the microbial phylogenetic network

Abstract

It has previously been suggested that the phylogeny of microbial species might be better described as a network containing vertical and horizontal gene transfer (HGT) events. Yet, all phylogenetic reconstructions so far have presented microbial trees rather than networks. Here, we present a first attempt to reconstruct such an evolutionary network, which we term the "net of life". We use available tree reconstruction methods to infer vertical inheritance, and use an ancestral state inference algorithm to map HGT events on the tree. We also describe a weighting scheme used to estimate the number of genes exchanged between pairs of organisms. We demonstrate that vertical inheritance constitutes the bulk of gene transfer on the tree of life. We term the bulk of horizontal gene flow between tree nodes as "vines", and demonstrate that multiple but mostly tiny vines interconnect the tree. Our results strongly suggest that the HGT network is a scale-free graph, a finding with important implications for genome evolution. We propose that genes might propagate extremely rapidly across microbial species through the HGT network, using certain organisms as hubs.

Figure 1.

Distribution of HGT vine widths.

Figure 2.

Connectivity of the HGT network.

Figure 3.

Three-dimensional representation of the net of life. The tree backbone was generated by using the average gene similarity approach (see Methods). The root is represented as a yellow sphere. Bacteria are shown as nodes on cyan branches; Archaea, as nodes on green branches. Red lines correspond to the vines representing HGT. The radius of the nodes is proportional to the estimated gene content size (in terms of number of gene families). Also, the widths of both the vertical inheritance branches and the horizontal inheritance vines correspond to the numbers of gene families transferred by either mechanism. For visualization purposes, only values for HGT vine width >30 are shown. Certain key species and taxa are labeled; for full names, please refer to Supplemental material.