Horizontal gene transfer in eukaryotes: the weak-link model

Abstract

The significance of horizontal gene transfer (HGT) in eukaryotic evolution remains controversial. Although many eukaryotic genes are of bacterial origin, they are often interpreted as being derived from mitochondria or plastids. Because of their fixed gene pool and gene loss, however, mitochondria and plastids alone cannot adequately explain the presence of all, or even the majority, of bacterial genes in eukaryotes. Available data indicate that no insurmountable barrier to HGT exists, even in complex multicellular eukaryotes. In addition, the discovery of both recent and ancient HGT events in all major eukaryotic groups suggests that HGT has been a regular occurrence throughout the history of eukaryotic evolution. A model of HGT is proposed that suggests both unicellular and early developmental stages as likely entry points for foreign genes into multicellular eukaryotes.

Keywords: endosymbiosis; eukaryotic evolution; gene acquisition; genome evolution; organellar gene transfer.

Figure 1

Illustration of the weak-link model of HGT. The unicellular or early developmental stages (spore, zygotes, embryos, etc.) are exposed to foreign genes. These weakly protected stages allow the entry and integration of foreign genes. A: In unicellular eukaryotes, foreign genes may be directly transmitted to offspring through mitosis. B: In multicellular eukaryotes with sexual reproduction, cell proliferation and differentiation spread the foreign genes to all cells including germ cells, which then give rise to male and female gametes. Subsequent fertilization allows foreign genes to be transmitted to offspring. C: In asexual multicellular eukaryotes, propagation of cells carrying foreign genes allows the foreign genes to be transmitted to offspring.