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.

Highlights

  • Horizontal gene transfer (HGT) is traditionally considered to be rare in multicellular eukaryotes such as animals

  • Because eukaryotic photosynthesis is derived from a primary endosymbiosis with a cyanobacterium as well as secondary and tertiary endosymbioses with miscellaneous algae [9,10,11,12], these genes are frequently interpreted as relicts of earlier cyanobacterial/algal endosymbionts and, evidence of plastid losses in some aplastidic eukaryotes [13,14,15]

  • Algae-related genes identified in C. intestinalis and other animals The annotated genome of C. intestinalis consists of 14,002 protein-coding genes and genome screening using AlienG [23] identified 169 of them as candidates of algal origin

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Summary

Introduction

Horizontal gene transfer (HGT) is traditionally considered to be rare in multicellular eukaryotes such as animals. 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. Gene transfer, including those occurred horizontally between distinct species (horizontal gene transfer, HGT) or those intracellularly from organelles (mitochondria or plastids) to the nucleus (endosymbiotic gene transfer, EGT), has been widely recognized as an important force in organismal and genome evolution [1,2,3]. As eukaryotic photosynthesis spans multiple major lineages whose relationships critically rely on the plastid existence in them [16,17,18], an accurate understanding of the distribution and origin of algal genes in eukaryotes is essential

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