Bacterial genes in eukaryotes: Relatively rare but real and important (<scp>C</scp>omment on <scp>DOI</scp> 10.1002/bies.201300095)

In an article in this issue of BioEssays, Schönknecht, Weber, and Lercher summarize the evidence of horizontal gene transfer (HGT) in eukaryotes, making a strong case for the importance of lineage-specific acquisition of bacterial genes for the adaptation of eukaryotes to specific lifestyles 1. In prokaryotes, HGT is the dominant mode of evolution; hence a network becomes a more adequate representation of evolution than a tree 2. Eukaryotes differ, conceivably thanks to the emergence of the nucleus – a barrier to foreign DNA – and the soma-germline separation that further curtailed HGT. Somewhat paradoxically, massive HGT, or more precisely, amalgamation of two distinct gene sets (from the alpha-proteobacterial symbiont that became the mitochondrion, and from its Archaea-like host) lies at the very root of the eukaryotic domain. Furthermore, massive HGT of cyanobacterial genes into the genome of the common ancestor of plants and algae accompanied the origin of the chloroplast. However, apart from these ancient cases of massive HGT, attempts to detect acquisition of bacterial genes by individual groups of eukaryotes have, until recently, largely been a frustrating pursuit. Most conspicuous is the report – in the iconic paper on the draft human genome sequence 3 – of approximately 100 genes inferred to have been acquired by vertebrates from bacteria. Most of these cases of purported HGT turned out to be false positives, caused primarily by the inadequate sampling of eukaryotic genomes available at the time and the apparent gross underestimate of the prevalence of lineage-specific gene loss 4. Schönknecht and co-workers capitalize on their recent analysis of the genome of the thermoacidophilic red alga Galdieria sulphuraria, in which 337 strong HGT candidates have been detected, by careful phylogenetic analysis including rigorous statistical test of phylogenetic tree topology. Strikingly, many of these genes appear to contribute directly to the adaption of this alga to an extreme lifestyle that is highly unusual among eukaryotes but common to numerous bacteria 5. Summarizing the results of phylogenomic analysis of eukaryotic genomes, Schönknecht et al. present data on HGT candidates in over 20 eukaryotes. The estimates widely vary, but in most cases, are modest: typically far below 1% of the genes in the respective genomes. Striking exceptions include bdelloid rotifers, asexual eukaryotes in which up to 10% of the genes seem to come from bacteria. The drastic differences in estimated HGT rates between eukaryotic groups appear to stem both from the genuine differences in lifestyles, and from methodological problems: many analyses were designed to detect only relatively recent HGT events. Generally, the available estimates are considered to represent the lower limit to lineage-specific HGT. Evidence of adaptive importance of the acquired genes is available for several eukaryotes in addition to G. sulphuraria. Since the rather ill-fated report of HGT candidates in the human genome 3, the study of lineage-specific HGT in eukaryotes has come full circle. Although most – if not all – of the original candidates appear false, the phenomenon itself turns out to be real and biologically important, even if not overwhelming quantitatively. Vertebrates are so far not in the list of recipients of bacterial HGT, but one wonders what more comprehensive phylogenomic analysis could reveal.