The scale and evolutionary significance of horizontal gene transfer in the choanoflagellate Monosiga brevicollis

Abstract

Background: It is generally agreed that horizontal gene transfer (HGT) is common in phagotrophic protists. However, the overall scale of HGT and the cumulative impact of acquired genes on the evolution of these organisms remain largely unknown.

Results: Choanoflagellates are phagotrophs and the closest living relatives of animals. In this study, we performed phylogenomic analyses to investigate the scale of HGT and the evolutionary importance of horizontally acquired genes in the choanoflagellate Monosiga brevicollis. Our analyses identified 405 genes that are likely derived from algae and prokaryotes, accounting for approximately 4.4% of the Monosiga nuclear genome. Many of the horizontally acquired genes identified in Monosiga were probably acquired from food sources, rather than by endosymbiotic gene transfer (EGT) from obsolete endosymbionts or plastids. Of 193 genes identified in our analyses with functional information, 84 (43.5%) are involved in carbohydrate or amino acid metabolism, and 45 (23.3%) are transporters and/or involved in response to oxidative, osmotic, antibiotic, or heavy metal stresses. Some identified genes may also participate in biosynthesis of important metabolites such as vitamins C and K12, porphyrins and phospholipids.

Conclusions: Our results suggest that HGT is frequent in Monosiga brevicollis and might have contributed substantially to its adaptation and evolution. This finding also highlights the importance of HGT in the genome and organismal evolution of phagotrophic eukaryotes.

Figure 1

Molecular phylogenies of bacterial or algal genes in M. brevicollis . A. L-threonine 3-dehydrogenase (GenBank accession number: XP_001746273). B. D-beta-hydroxybutyrate dehydrogenase (GenBank accession number: XP_001744068). C. Metallo-beta-lactamase (GenBank accession number: XP_001747251). D. L-galactono-1,4-lactone dehydrogenase (GenBank accession number: XP_001748157). Numbers associated with branches show bootstrap values from maximum likelihood and distance analyses, respectively. Asterisks indicate bootstrap values lower than 50%. Taxonomic affiliations are shown after genus names, with choanoflagellates bolded.

Figure 2

Evaluation of three computational programs on prediction of prokaryotic and algal genes in M. brevicollis .ÉFor AlienG, the alien index threshold was set to 1.2. For PhyloGenie, bootstrap value threshold for interested branches was set to 50%. Prediction results from three programs are shown in three different colors. The percentages in white ovals indicate positive rates (before hyphen) and false negative rates (after hyphen). The percentage in colored background indicates the positive rate for each part and is shown above. The numbers of foreign genes identified by manual curation (before slash) and originally predicted (after slash) are shown below.

Figure 3

Functional categories for genes acquired from algae and bacteria in M. brevicollis .