Horizontal gene transfer between bacteria and animals

Abstract

Horizontal gene transfer is increasingly described between bacteria and animals. Such transfers that are vertically inherited have the potential to influence the evolution of animals. One classic example is the transfer of DNA from mitochondria and chloroplasts to the nucleus after the acquisition of these organelles by eukaryotes. Even today, many of the described instances of bacteria-to-animal transfer occur as part of intimate relationships such as those of endosymbionts and their invertebrate hosts, particularly insects and nematodes, while numerous transfers are also found in asexual animals. Both of these observations are consistent with modern evolutionary theory, in particular the serial endosymbiotic theory and Muller's ratchet. Although it is tempting to suggest that these particular lifestyles promote horizontal gene transfer, it is difficult to ascertain given the nonrandom sampling of animal genome sequencing projects and the lack of a systematic analysis of animal genomes for such transfers.

Figure 1. Illustration of HGT from bacteria to animals described in the main text

HGT events from bacteria to animals are illustrated by blue arrows with the width representing the abundance of transfers. Organelle transfers (chloroplast, green; mitochondria, red) are shown at the base of the appropriate lineage. Transfers from bacteria that cannot be attributed to a specific bacterial lineage are shown as arising from the middle of the Eubacteria branch. Other types of HGT are not shown, including eukaryote-to-bacteria transfers and transfers from bacteria to eukaryotes other than animals. The tree itself is used only for illustration purposes and does not accurately reflect a true phylogeny. The phylogeny of the eukaryotic and eubacterial lineages as well as issues related to resolving particular lineages is described elsewhere (e.g. [58]).

Figure 2. Endosymbiont HGT ratchet

A HGT ratchet has been proposed [15] to explain the accumulation of nuclear genes of organelle origin. This model can be extended to include HGT involving endosymbionts. At low frequency, a gene (red) is transferred from the endosymbiont genome (green circular chromosome) to the nuclear genome (gray linear chromosomes) (A). With some even lower frequency, such transfers will occur in a manner which will allow the gene to be functional in its new location. Subsequently, either the nuclear or endosymbiont version will be lost. Loss of the endosymbiont version is nearly irreversible and as such the gene becomes fixed in the nuclear genome (B). Loss of the nuclear version returns the endosymbiont to its original state and the process can repeat itself (C). The result is that over time, all of the genes that can insert into the nuclear genome will do so. When maintenance of endosymbiont structure is not essential and the HGT now fulfills all of the needs of the host, the endosymbiont becomes obsolete and can also be lost (D).