Ancient gene transfer from algae to animals: Mechanisms and evolutionary significance

Abstract

BackgroundHorizontal gene transfer (HGT) is traditionally considered to be rare in multicellular eukaryotes such as animals. Recently, many genes of miscellaneous algal origins were discovered in choanoflagellates. Considering that choanoflagellates are the existing closest relatives of animals, we speculated that ancient HGT might have occurred in the unicellular ancestor of animals and affected the long-term evolution of animals.ResultsThrough genome screening, phylogenetic and domain analyses, we identified 14 gene families, including 92 genes, in the tunicate Ciona intestinalis that are likely derived from miscellaneous photosynthetic eukaryotes. Almost all of these gene families are distributed in diverse animals, suggesting that they were mostly acquired by the common ancestor of animals. Their miscellaneous origins also suggest that these genes are not derived from a particular algal endosymbiont. In addition, most genes identified in our analyses are functionally related to molecule transport, cellular regulation and methylation signaling, suggesting that the acquisition of these genes might have facilitated the intercellular communication in the ancestral animal.ConclusionsOur findings provide additional evidence that algal genes in aplastidic eukaryotes are not exclusively derived from historical plastids and thus important for interpreting the evolution of eukaryotic photosynthesis. Most importantly, our data represent the first evidence that more anciently acquired genes might exist in animals and that ancient HGT events have played an important role in animal evolution.

Widespread impact of horizontal gene transfer on plant colonization of land

“…These viral and bacterial genes were integrated into mitochondria and passed onto descendants ultimately through the apical meristem. Such observations, combined with other relatively recent HGT events reported in plants1317 and animals161846, suggest that neither germline nor apical meristem constitutes an insurmountable barrier to HGT.…”

An Ancient Relative of Cyclooxygenase in Cyanobacteria Is a Linoleate 10S-Dioxygenase That Works in Tandem with a Catalase-related Protein with Specific 10S-Hydroperoxide Lyase Activity

“…As Ni et al (46) conclude, "Most identified algal genes (identified by the authors as potential transfers from alga/ cyanobacteria to Ciona intestinalis) are related to molecule transport and signaling, suggesting their important role in intercellular communication and possibly the origin of multicellularity in animals." The fatty acid heme dioxygenases and cyclooxygenases certainly fit into the categories of signaling and intercellular communication.…”

Origin of chordate peptides by horizontal protozoan gene transfer in early metazoans and protists: Evolution of the teneurin C-terminal associated peptides (TCAP)

“…As the first heterotrophic (non-phototrophic) multicellular organisms evolved, prokaryotes and protists would have been the fundamental nutrient sources. Choanoflagellates, are thought to be the most closely related protist lineage to the metazoan (King et al, 2008;Ni et al, 2012;Ra, 2012;Tucker, 2013;Tucker et al, 2012). However, considerable controversy exists for the phylogenetic relationships of the basal metazoans.…”