Horizontal gene transfer as the source of evolutionary innovation in eukaryotes

PROJECT SUMMARY
Horizontal gene transfer (HGT) represents a dominant force in bacterial evolution, however its role in shaping
the evolutionary processes in eukaryotic genomes has been a subject of intense debate. Class Bdelloidea of the
phylum Rotifera, a large invertebrate taxon comprising close to 500 described species, has so far withstood any
challenges questioning the massive amounts of HGT from non-metazoan sources reported in their genomes,
and remain the record-holders among Metazoa with regard to the proportion of foreign genes, with HGT
candidates comprising at least 8% of all coding sequences. Many of them have acquired spliceosomal introns
and occur in quartets, which is indicative of their arrival prior to whole-genome duplication over 60 million years
ago in the common ancestor of bdelloids. Others apparently represent more recent arrivals, lacking introns and
favoring subtelomeric localization, and may not reach fixation. While the ability to capture and retain foreign
genes has been the distinguishing characteristic of the bdelloid lineage since its divergence from the sister
classes, its continuous dynamics over time has not been analyzed in a systematic fashion, due to the
incompleteness of distal chromosome regions in comparison with the core genome. The ancient HGT events,
which have been maintained by purifying selection throughout the course of bdelloid evolution, can be regarded
as selectively advantageous for the entire taxon, however their molecular function cannot always be inferred on
the basis of homology alone. In this proposal, we seek to investigate both recent and ancient HGT cases, in
aggregate and individually. A glimpse into population-wide distribution of recent HGT cases in Aim 1 is expected
to uncover their short-term adaptive value in processes such as adaptation to dietary preferences or toxic
substances in changing environments and shed light on the mechanisms of their recent acquisition. An in-depth
look into taxon-wide establishment of ancient HGT events from bacteria and fungi, in Aims 2 and 3 respectively,
should clarify the value of these acquisitions for bdelloids and their footprint on their evolutionary history, by
zeroing in on molecular underpinnings of the functional role of these proteins in diverse taxa, including
pathogenic fungi where some of these genes may represent therapeutic targets.

Grant Number: 5R01GM111917-12
NIH Institute/Center: NIH
Principal Investigator: Irina Arkhipova