The complexity of virus systems: the case of endosymbionts

Abstract

Host-microbe symbioses involving bacterial endosymbionts comprise some of the most intimate and long-lasting interactions on the planet. While restricted gene flow might be expected due to their intracellular lifestyle, many endosymbionts, especially those that switch hosts, are rampant with mobile DNA and bacteriophages. One endosymbiont, Wolbachia pipientis, infects a vast number of arthropod and nematode species and often has a significant portion of its genome dedicated to prophage sequences of a virus called WO. This phage has challenged fundamental theories of bacteriophage and endosymbiont evolution, namely the phage Modular Theory and bacterial genome stability in obligate intracellular species. WO has also opened up exciting windows into the tripartite interactions between viruses, bacteria, and eukaryotes.

Figure 1

Effects of microbial ecology on exposure to phage gene pools. Facultative intracellular bacteria have the largest exposure to bacteriophage genes due to their flexible lifestyle involving both the free-living and intracellular environments; thus, they have the greatest amount of mobile DNA in their genomes. Extracellular bacteria have an intermediate amount of mobile DNA, while obligate intracellular bacteria have the least. However, intracellular bacteria that switch hosts and can be horizontally transmitted often retain a large quantity of mobile DNA including phages.

Figure 2

WO particle and genome structure. (A) Typical appearance of a tailed bacteriophage, color-coded by structural groups. (B) Electron micrograph of WO particles. Examples of phage particles are indicated with arrowheads. Shown is WO isolated from wCauB in the moth Ephestia kuehniella. Photo courtesy of Sarah Bordenstein. (C) The modular genome of prophage WO. Relative portions of the genome dedicated to individual modules and the modules’ orientation and arrangement are shown for lysogenic WOCauB2. Other WO strains have modules in differing arrangements and orientations and some may lack various modules all together. Not all genes are shown.

Figure 3

Evolution of bacteriophages in endosymbionts and free-living bacteria. Bacteriophages (1) of endosymbionts (2) are restricted in their interactions with other phages due to the barrier of the eukaryotic host membrane (3). Their genomes evolve mainly through recombination (4), point mutation (5), and deletion (6). Bacteriophages (7) of free-living bacteria (8) can more freely interact with each other facilitating modular gene exchange (9) and forming viruses consisting of parts of each parent strain (10). Thus, free-living but not endosymbiont phages evolve by the Modular Theory.

Figure 4

Examples of gene flow between WO, Wolbachia, and insects. WO prophage sequences (1) have been transferred between coinfections of different Wolbachia strains (2 and 3) on several occasions. Additionally, Wolbachia genes have been transferred to a Rickettsia plasmid (4), and both WO and Wolbachia genes have been found in multiple insect host genomes (5).