Horizontal gene transfer in the sponge Amphimedon queenslandica

Abstract

Horizontal gene transfer (HGT) is the nonsexual transfer of genetic sequence across species boundaries. Historically, HGT has been assumed largely irrelevant to animal evolution, though widely recognised as an important evolutionary force in bacteria. From the recent boom in whole genome sequencing, many cases have emerged strongly supporting the occurrence of HGT in a wide range of animals. However, the extent, nature and mechanisms of HGT in animals remain poorly understood. Here, I explore these uncertainties using 576 HGTs previously reported in the genome of the demosponge Amphimedon queenslandica.The HGTs derive from bacterial, plant and fungal sources, contain a broad range of domain types, and many are differentially expressed throughout development. Some domains are highly enriched; phylogenetic analyses of the two largest groups, the Aspzincin_M35 and the PNP_UDP_1 domain groups, suggest that each results from one or few transfer events followed by post-transfer duplication. Their differential expression through development, and the conservation of domains and duplicates, together suggest that many of the HGT-derived genes are functioning in A. queenslandica. The largest group consists of aspzincins, a metallopeptidase found in bacteria and fungi, but not typically in animals. I detected aspzincins in representatives of all four of the sponge classes, suggesting that the original sponge aspzincin was transferred after sponges diverged from their last common ancestor with the Eumetazoa, but before the contemporary sponge classes emerged. In A. queenslandica, the aspzincins may have been co-opted for multiple functions, since 54 of the 90 fit into one of four ontogenetic expression profiles, each of which is putatively co-expressed with different suites of native genes. Based on secretion signals and the conservation of key catalytic residues, I propose that proteolytic activity is maintained in at least one of the aspzincin roles in A. queenslandica.Mobile elements are capable of genomic excision, movement and integration, they enable HGT in bacteria, and some animal HGTs are genomically close to eukaryotic transposable elements (TEs); as such, mobile elements are speculated as possible players in the mechanisms of interkingdom and interdomain HGT to animals. In A. queenslandica, the overall repeats densities around predicted unduplicated HGTs are not different to those around predicted unduplicated native genes. However, the surrounding repeats content of unduplicated HGTs has slightly increased proportions of the helitron DNA transposon and of simple repeats. Further, 29% of the HGT-derivatives are TEs, half of which are unknown in class, a quarter are copia long terminal repeats retrotransposons and the other quarter are helitrons. These data suggest that repeats and TEs may have putative roles in the HGT process in animals, such as simple repeats possibly conferring increased chances of genomic integration through recombination and helitrons perhaps increasing chances of HGT functionality via their reservoir of regulatory elements. Another seven per cent of the HGT-derivatives have high sequence similarities to proteins present on bacterial plasmids, suggestive that plasmids were involved in some of the transfers. Together, these results offer novel insight on HGT in A. queenslandica and demonstrate that HGT has a varied nature in this animal with an extensive impact, partially due to post-transfer duplications. Further, this work offers insights on possible mechanisms that led to the HGT derived genes of this sponge.