Abstract
By manipulating arthropod reproduction worldwide, the heritable endosymbiont Wolbachia has spread to pandemic levels. Little is known about the microbial basis of cytoplasmic incompatibility (CI) except that bacterial densities and percentages of infected sperm cysts associate with incompatibility strength. The recent discovery of a temperate bacteriophage (WO-B) of Wolbachia containing ankyrin-encoding genes and virulence factors has led to intensifying debate that bacteriophage WO-B induces CI. However, current hypotheses have not considered the separate roles that lytic and lysogenic phage might have on bacterial fitness and phenotype. Here we describe a set of quantitative approaches to characterize phage densities and its associations with bacterial densities and CI. We enumerated genome copy number of phage WO-B and Wolbachia and CI penetrance in supergroup A- and B-infected males of the parasitoid wasp Nasonia vitripennis. We report several findings: (1) variability in CI strength for A-infected males is positively associated with bacterial densities, as expected under the bacterial density model of CI, (2) phage and bacterial densities have a significant inverse association, as expected for an active lytic infection, and (3) CI strength and phage densities are inversely related in A-infected males; similarly, males expressing incomplete CI have significantly higher phage densities than males expressing complete CI. Ultrastructural analyses indicate that approximately 12% of the A Wolbachia have phage particles, and aggregations of these particles can putatively occur outside the Wolbachia cell. Physical interactions were observed between approximately 16% of the Wolbachia cells and spermatid tails. The results support a low to moderate frequency of lytic development in Wolbachia and an overall negative density relationship between bacteriophage and Wolbachia. The findings motivate a novel phage density model of CI in which lytic phage repress Wolbachia densities and therefore reproductive parasitism. We conclude that phage, Wolbachia, and arthropods form a tripartite symbiotic association in which all three are integral to understanding the biology of this widespread endosymbiosis. Clarifying the roles of lytic and lysogenic phage development in Wolbachia biology will effectively structure inquiries into this research topic.
Highlights
Wolbachia are a–proteobacterial endosymbionts that are recognized for their widespread distribution and inductions of reproductive parasitism, including feminization, malekilling, parthenogenesis, and cytoplasmic incompatibility (CI) in arthropods [1]
WO-B [44] based on this speculation is that the host, rather than Wolbachia, benefits from the presence of a lytic phage since host level and phage level selection could both favor an active bacteriophage infection that lyses Wolbachia cells and reduces the bacterial load in the arthropod host
The results presented here raise the interesting possibility that common environmental or host genetic factors known to modulate
Summary
Wolbachia are a–proteobacterial endosymbionts that are recognized for their widespread distribution and inductions of reproductive parasitism, including feminization, malekilling, parthenogenesis, and cytoplasmic incompatibility (CI) in arthropods [1]. Sex-specific expression of two phage-associated genes has been observed [29,47] For these reasons, bacteriophage WO-B has been tentatively proposed as a genetic candidate for inducing CI [29,42,48], but there is inconsistent evidence on whether WO-B sequence diversity correlates with CI crossing type [49,50]. The flowchart is based on the following hypothesis: if lytic development of temperate phage WO-B leads to bacterial lysis or slowed cell divisions, the relative copy number of phages per bacterium may negatively associate with the relative copy number of Wolbachia per host, which in turn is well established to positively associate with CI levels.
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
