Horizontal gene transfer and the unusual genomic architecture of bdelloid rotifers

Abstract

Bdelloid rotifers are microscopic aquatic animals, notable for their ancient asexuality and their extreme desiccation tolerance. In the absence of sexual reproduction, bdelloids have persisted for over 40 million years, diverging into >450 morphologically distinct species. Despite the two-fold cost of sex, asexual lineages tend to be short-lived and species poor. Many theories exist to explain the success of sexual reproduction, and in the light of these, ancient asexual lineages are an evolutionary paradox. Understanding the persistence and speciation of ancient asexuals may provide clues to factors underlying the success of sexual reproduction.

Bdelloid rotifers have unusual genomic features that may have provided some compensation for their long-term absence of sexual reproduction. Here I focus on two: multiple gene copies and horizontal gene transfer (HGT).

Bdelloids have multiple copies of many genes, and are considered degenerate tetraploids. In genomes influenced by the opposing forces of gene conversion and divergence of former alleles, I examine the relationships between, and biochemical implications of divergence of a multi-gene family of alpha tubulin.

Horizontally acquired genes were initially identified in sub-telomeric regions of two species of bdelloid rotifer. In order to understand what role foreign genes might have played in bdelloid evolution we need to examine the extent, frequency and mechanism of HGT. Here I develop a bioinformatics pipeline for identifying horizontally acquired genes in transcriptomes. By comparing HGT in a number of bdelloid species I demonstrate that the majority of transcribed foreign genes were acquired before the divergence of extant bdelloid species, but the presence of more recently acquired genes implies that HGT is ongoing. By comparing the extent of HGT in closely related species with different desiccation frequencies I provide initial support for the hypothesis that bdelloid HGT is facilitated by DNA breakage and repair during cycles of desiccation and rehydration.