Recruitment of Mobile Genetic Elements for Diverse Cellular Functions in Prokaryotes

Abstract

Prokaryotic genomes are replete with mobile genetic elements (MGE) that span a continuum of replication autonomy. On numerous occasions during microbial evolution, diverse MGE lose their autonomy altogether but, rather than being quickly purged from the host genome, assume a new function that benefits the host, rendering the immobilized MGE subject to purifying selection, and resulting in its vertical inheritance. This mini-review highlights the diversity of the repurposed (exapted) MGE as well as the plethora of cellular functions that they perform. The principal contribution of the exaptation of MGE and their components is to the prokaryotic functional systems involved in biological conflicts, and in particular, defense against viruses and other MGE. This evolutionary entanglement between MGE and defense systems appears to stem both from mechanistic similarities and from similar evolutionary predicaments whereby both MGEs and defense systems tend to incur fitness costs to the hosts and thereby evolve mechanisms for survival including horizontal mobility, causing host addiction, and exaptation for functions beneficial to the host. The examples discussed demonstrate that the identity of an MGE, overall mobility and relationship with the host cell (mutualistic, symbiotic, commensal, or parasitic) are all factors that affect exaptation.

Keywords: antivirus defense mechanisms; biological conflict systems; exaptation; horizontal gene transfer; mobile genetic element.

FIGURE 1

Entire mobile genetic elements double as defense systems. Autonomous MGEs, such as bacteriophages, plasmids, transposons and retrons, encode genes that defend the host cells against invasion by related or unrelated MGEs (A–D). For example, trbK encoded by the broad host range plasmid RP4 excludes plasmid R702. Such defense-related genes are frequently shuttled back and forth between MGEs and their host cells, such as, for example, the Old family nuclease encoded by phage P2.

FIGURE 2

Proteins involved in DNA replication, recombination and repair freelance between MGEs and cells. Homologous resolvases mediate the resolution of both MGE and chromosome replication intermediates (A). DNA inverting serine recombinases direct the expression of alternative phage tail fiber genes or host flagellum genes (B). Exapted bacteriophage genes endow the host DNA repair pathways via homologous recombination (C) or nonhomologous end-joining (D).

FIGURE 3

Recruitment of transcription factors from MGEs to regulate host gene expression. One example is Ner, which contains an Xre-family HTH domain and regulates the lysis-lysogeny switch of bacteriophage Mu (A). The amino acid sequence of Ner is 68% identical to the maltose operon-activating transcription factor SfsB, indicating the recent recruitment of a Ner homolog for the regulation of host carbon metabolism (B). Xre domains are widespread in antitoxin proteins, such as HipB, which autoregulate their own expression and the expression of other host genes (C). Antitoxins often disassociate from their TA operons and assume dedicated roles as transcription factors (D).

FIGURE 4

Multiple contributions of distinct mobile genetic elements to intercellular transfer pathways and eukaryogenesis. Exaptations of toxin-antitoxins (TAs), integrative and conjugative elements (ICE), bacterial retrotransposons and double-stranded DNA bacteriophages are diagrammed. An RNA-cleaving toxin apparently was incorporated into the eukaryotic nonsense-mediated RNA decay system. The conjugation apparatus of ICE was exapted for the transfer of proteins (type 4 secretion systems). Recruitment of the reverse transcriptase from bacterial retrotransposons yielded the key component of the eukaryotic spliceosome, Prp8 (accompanied by inactivation of the reverse transcriptase), as well as telomerases which retain the activity. The structural module of double-stranded DNA bacteriophages was repurposed for the delivery of proteins (type 6 secretion systems) or host DNA (GTAs) between cells. The replication and lysis modules donated multiple genes that play diverse roles in both prokaryotes and eukaryotes.