Symbiotic enemies fight over insect

Phage and Wolbachia form tug of war to influence arthropod reproduction

By Clementine Wallace | May 23, 2006

Wolbachia, a common bacteria, manipulates reproduction in arthropods -- but may sometimes fight for the right to do so with its bacteriophage, according to a study published in this week's PLoS Pathogens. In insects, Wolbachia induce cytoplasmic incompatibility (CI), in which infected males are unable to mate with uninfected females. Previous research has shown that the higher the density of Wolbachia, the stronger the CI. The latest findings show that CI strength is also related -- albeit, inversely -- to the density of a Wolbachia phage. "We observed that the more phages proliferate, the less prevalent the bacteria, and the less CI occurs," lead author Seth Bordenstein, from the Marine Biological laboratory in Woods Hole, MA, told The Scientist. "In the end, it's as if the phage is in a tug of war with Wolbachia." Present in 75% of all insects, Wolbachia are one of the most widespread reproductive parasites in the biosphere. They are maternally inherited and infect male gonadic tissues, where they encrypt sperm with a modification that prevents them from producing viable offspring with uninfected females. "On the other hand, when both infected males and females mate, their eggs are viable," said Bordenstein. "From the Wolbachia's perspective, this is great -- it hijacks the insect's reproductive system to ensure its own spread through infected females." However, infected males and uninfected females can sometimes produce viable offspring. Although researchers have been studying CI for the past 50 years, the microbial and viral factors that shape this variability remain unclear. Working with the well-studied wasp Nasonia vitripennis, the team used quantitative PCR to enumerate Wolbachia bacteriophages (WO-B) and Wolbachia in vivo, and related these densities to CI levels observed in the wasp. They found that phage density is inversely associated to bacterial density and to CI. The researchers also performed ultrastructural analyses using Transmission Electron Microscopy, and saw virus particles inside the bacteria, some of them lysing and exiting cells. However, the ways in which the phage might actually be influencing CI remain unclear. Bordenstein and his colleagues demonstrate phage affects CI indirectly, during the lytic stage, when the virus is no longer expressed but spreading. Other studies have suggested the phage might also be acting through the expression of some genes during its lysogenic state, when it integrates its genome inside the bacteria's DNA. "One model doesn't exclude the others, and it could be that all models coexist -- the system is rich with unanswered questions," said Bordenstein. For instance, he argued that it's important to clarify the separate roles played by the lytic and the lysogenic stages in phage development. "This inverse correlation [between phage density and CI] is what you can expect to observe if indeed the lytic phage particles are killing Wolbachia cells and develop a density model of CI," Steven Sinkins, from the University of Oxford in the UK, who was not involved in the research, told The Scientist. "But there seems to be a threshold above which Wolbachia densities no longer influence the expression of CI, so in many cases the density model will not apply -- it depends on the strain and the host." Last year, Sinkins and his colleagues published a study showing that a gene in the phage genome correlated with the CI phenotype, suggesting that the phage could be directly involved in CI. "But still much research remains to be done to figure out how the phage's sequence might be influencing CI in different systems," Stephen Dobson from the University of Kentucky, also not a co-author, told The Scientist. "What is apparent is the complexity of the emerging story of multi-layered symbioses." Clementine Wallace Links within this article D. Secko, "A sleek genome, except for all the junk." The Scientist, April 12, 2004. Seth Bordenstein et al. "The tripartite association between bacteriophage, Wolbachia and arthropods," PLoS Pathogens, published online May 19, 2006. K. Lee, "Speciation induced by bacterial symbiont?" The Scientist, February 8, 2001. Seth Bordenstein Steven Sinkins Sinkins SP et Al. "Wolbachia variability and host effects associated with crossing type in Culex mosquitoes," Nature, July 14, 2005. PM_ID: 16015330 Stephen Dobson Sanogo YO, Eitam A, Dobson SL. "No evidence for bacteriophage WO orf7 correlation with Wolbachia induced cytoplasmic incompatibility in the Culex pipiens complex," Journal of Medical Entomology, September 2005. PM_ID: 16365997

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