Trends in Microbiology
ReviewPhage WO of Wolbachia: lambda of the endosymbiont world
Section snippets
Mobile elements in intracellular bacteria
The restrictive lifestyle of obligate intracellular bacteria can lead to a near minimal genome state that encodes only essential functions. This reduction is associated with a genome-wide deletion bias, population bottlenecks and relaxed selection as a result of the ability of the bacterium to acquire nutrients from the host cell rather than synthesize them itself 1, 2. As a consequence of reductive evolution, mobile DNA elements have often been shown to be rare or absent from such streamlined
The biology of bacteriophage WO
Wolbachia species are members of the obligate intracellular Rickettsiales and forge parasitic relationships with arthropods and mutualistic relationships, primarily with nematodes. During their 100-million-year association with their hosts, the maternally transmitted bacteria have evolved as “reproductive parasites” that cause cytoplasmic incompatibility (CI), feminization, parthenogenesis and male killing in arthropods, whereas in nematodes and some arthropods, they are mutualistic and can be
Evolution of the WO core genome
In dsDNA phages of bacteria with a free-living replicative stage, evolution is categorized by the Modular Theory 32, 36, 37. According to this theory, a phage genome can be divided into functional units or modules (each one responsible for functions such as head or tail formation, lysis, lysogeny), which can be mixed by recombination with other phages. Each module often comprises genes that have a shared evolutionary history owing to their physical linkage and functional co-adaptation.
Lifecycle of phage WO
Although the lytic and lysogenic nature of temperate phage WO has been demonstrated, the genetic mechanisms that drive prophage induction and lytic activity are currently unknown. Phage particles have been visualized for several Wolbachia strains (Table 1) but the precise identification of phage termini has occurred only from phages of the Wolbachia infection of Cadra cautella moths [29]. A serine recombinase gene homolog that is probably responsible for integration of these phages is located
Effectors, toxins and the tripartite relationship of WO, Wolbachia and arthropods
In addition to the genomics and transmissibility of bacteriophage WO, there is considerable interest in the phage's function in the Wolbachia–arthropod symbiosis. Mobile elements were initially hypothesized to be responsible for causing reproductive parasitism because they can promiscuously transfer new functions between strains, potentially explaining the phylogenetic curiosity that different types of reproductive parasitism (CI, male killing, feminization, parthenogenesis) do not cluster in
The Phage Density Model
Phage sequence analyses find no phylogenetic clustering of WO genotypes between the four major Wolbachia-induced sexual alterations. Further, there are some Wolbachia strains that induce CI, male killing or parthenogenesis but lack the WO prophage 23, 24. These facts led to the development of the Phage Density Model as an alternative, but not mutually exclusive, explanation for the role of phage WO in sexual alterations (Figure 3) [27]. This theory proposes that variations in phage lysis are
Biomedical applications for phage WO
Wolbachia has become increasingly important to human health and disease through two routes. First, vector control programs aimed at curbing the spread of insect-vectored diseases such as malaria and dengue fever will rely on the ability to release insect vectors transfected with Wolbachia infections that reduce the vectorial competence 69, 70, 71, 72, 73, 74. Second, the discoveries that river blindness, lymphatic filariasis [75] and heartworm [76] are associated with Wolbachia-induced
Concluding remarks and future directions
Studies of phage WO have shown its potential to have a substantial effect on the symbiosis between Wolbachia and host arthropods. Extrapolation of the phage infection frequency places WO in potentially millions of insect species, where it can contribute to Wolbachia genomic diversity and function in a number of ways, including horizontal gene transfer between different Wolbachia and between other endosymbionts, exchange of other mobile elements such as insertion sequences, intragenic
Acknowledgements
We thank Robert Brucker and Meghan Chafee for helpful feedback on the manuscript. This work was supported by grants NSF IOS-0852344 and NIH R01 GM085163-01 to S.R.B. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official view of the NSF or NIH.
Glossary
- Cytoplasmic incompatibility (CI)
- a sperm–egg incompatibility that renders embryos non-viable in crosses between infected males and uninfected females or females harboring a different strain of Wolbachia.
- Feminization
- the process by which infected male embryos are converted to morphological and functional females.
- Haplotype
- a distinct WO prophage type, based on nucleotide differences.
- Male killing
- the process by which male embryos or larvae are preferentially killed relative to female ones.
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