Evaluating the Evolutionary Origins of Unexpected Character Distributions within the Bacterial Planctomycetes-Verrucomicrobia-Chlamydiae Superphylum

Abstract

Recently, several characters that are absent from most bacteria, but which are found in many eukaryotes or archaea, have been identified within the bacterial Planctomycetes-Verrucomicrobia-Chlamydiae (PVC) superphylum. Hypotheses of the evolutionary history of such characters are commonly based on the inference of phylogenies of gene or protein families associated with the traits, estimated from multiple sequence alignments (MSAs). So far, studies of this kind have focused on the distribution of (i) two genes involved in the synthesis of sterol, (ii) tubulin genes, and (iii) c1 transfer genes. In many cases, these analyses have concluded that horizontal gene transfer (HGT) is likely to have played a role in shaping the taxonomic distribution of these gene families. In this article, we describe several issues with the inference of HGT from such analyses, in particular concerning the considerable uncertainty associated with our estimation of both gene family phylogenies (especially those containing ancient lineage divergences) and the Tree of Life (ToL), and the need for wider use and further development of explicit probabilistic models to compare hypotheses of vertical and horizontal genetic transmission. We suggest that data which is often taken as evidence for the occurrence of ancient HGT events may not be as convincing as is commonly described, and consideration of alternative theories is recommended. While focusing on analyses including PVCs, this discussion is also relevant for inferences of HGT involving other groups of organisms.

Keywords: LGT; PVC superphylum; gene duplication; gene loss; lateral gene transfer; phylogenetic estimation errors.

Figure 1

Influence of HGT, gene loss, and gene duplication on phylogenetic and taxonomic distribution of gene families. Three different hypothetical evolutionary scenarios are shown for gene family evolution within a simple four-taxon species tree: (i) in the absence of HGT, gene loss, or gene duplication, the gene tree has the same topology as the species tree (ii) a combination of HGT and gene loss yields a gene tree with a different topology to the species tree (iii) a combination of gene loss and gene duplication yields a gene tree with a different topology to the species tree, with the same gene tree topology as for scenario (ii).

Figure 2

Example phylogenetic tree considered to support a hypothesis of HGT involving PVC organisms. Tree is adapted based on Figure 5b of an analysis of sterol synthesis by Pearson et al. (2003). The tree was drawn using all bacterial oxidosqualene cyclase (OSC)-family sequences available in the public databases at the time of the analysis. Taxon labels indicate the genus from which the sequence was sampled. The “MetylSHC” label indicates a sequence taken from the bacterium Methylococcus capsulatus, and is a member of the squalene–hopene cyclase (SHC) gene family, which is related to the OSC family. All eukaryotic sequences are labeled in red, all non-PVC bacterial sequences are labeled in blue, the one PVC sequence is labeled in light blue with a dark blue background. The branch that partitions all eukaryotic sequences from all bacterial sequences is drawn thicker than all other branches in the tree.