INTRODUCTION
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Vertical gene inheritance is the main pathway of transmission of genomic information from the parents to their offspring via germline or cell division. However, genetic information can be transmitted also between organisms that are not directly related; these exchanges are termed horizontal gene transfer (HGT; also known as lateral gene transfer) (1). Among prokaryotes, HGT—first observed as the spreading of drug resistance within a bacterial population (2)—is now recognized as a major evolutionary force (3,-5). Indeed, several genome-wide studies have shown that HGT occurs at a high frequency between prokaryotic species, particularly if they are closely related or if they coexist in the same habitat or community, which provides many opportunities for DNA transfer (4, 5). Unlike evolution via gene duplications and mutations, a slow and incremental process, HGT permits fast acquisition of a new function important for species adaptation and survival.
Numerous cases of HGT from bacteria to eukaryotes have been demonstrated, although this process is assumed to be much less frequent than HGT between bacteria. The early evolution of eukaryotes was marked by endosymbiotic events leading to permanent acquisition of major organelles, e.g., mitochondria that originated from proteobacteria and plastids that originated from cyanobacteria, followed by organelle-to-nucleus gene transfer, usually referred to as endosymbiotic gene transfer (EGT) (6). Whereas the episodic gene transfer via EGT has a demonstrated evolutionary significance, the importance of HGT in the evolution of eukaryotes is still debated (7). A recent study analyzing a large number of protein sequences from bacterial and eukaryotic organisms indicates that gene inheritance in eukaryotes is predominantly vertical and suggests that HGT occurs only occasionally and that sequences acquired by HGT do not accumulate in eukaryotic genomes and do not contribute to long-term evolution of gene content (8). However, it is generally agreed that HGT from prokaryotes to eukaryotes does occur to a certain extent and, in some cases, plays a role in adaptive evolution (9). Whereas the identification of HGT genomic signatures indicates the existence of such events in the course of evolution, it does not inform about the pathway(s) and mechanisms(s) by which these sequences have been transferred. Instead, this information derives from numerous studies of known systems of natural and experimental gene transfer from bacteria to eukaryotic cells—such as the Agrobacterium-host plant interaction, the best-studied and best-understood system of transkingdom DNA transfer. Here, we review the major known cases of HGT from bacteria to eukaryotes that do not originate from prokaryote-derived permanent organelles, with a focus on natural and artificial prokaryote-to-eukaryote gene transfer systems that may help us understand the potential mechanisms involved in these transkingdom exchanges of genetic information.
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