1. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature. Lepage, D.*, J.A. Metcalf*, S.R. Bordenstein, J. On, J. Perlmutter, J.D. Shropshire, E. Layton, J. Beckmann, and S.R. Bordenstein (*Co-first authors) Select coverage:
Major point: Two genes, cifA and cifB, in the eukaryotic association module of prophage WO (related paper from the lab) enable Wolbachia to cause cytoplasmic incompatibility
Description: The genus Wolbachia is an archetype of maternally inherited intracellular bacteria that infect the germline of numerous invertebrate species worldwide. They can selfishly alter arthropod sex ratios and reproductive strategies to increase the proportion of the infected matriline in the population. The most common reproductive manipulation is cytoplasmic incompatibility, which results in embryonic lethality in crosses between infected males and uninfected females. Females infected with the same Wolbachia strain rescue this lethality. Despite more than 40 years of research and relevance to symbiont-induced speciation, as well as control of arbovirus vectors and agricultural pests, the bacterial genes underlying cytoplasmic incompatibility remain unknown. Here we use comparative and transgenic approaches to demonstrate that two differentially transcribed, co-diverging genes in the eukaryotic association module of prophage WO from Wolbachia strain wMel recapitulate and enhance cytoplasmic incompatibility. Dual expression in transgenic, uninfected males of Drosophila melanogaster crossed to uninfected females causes embryonic lethality. Each gene additively augments embryonic lethality in crosses between infected males and uninfected females. Lethality associates with embryonic defects that parallel those of wild-type cytoplasmic incompatibility and is notably rescued by wMel-infected embryos in all cases. The discovery of cytoplasmic incompatibility factor genes cifA and cifB pioneers genetic studies of prophage WO-induced reproductive manipulations and informs the continuing use of Wolbachia to control dengue and Zika virus transmission to humans.
2. Phylosymbiosis: Relationships and functional effects of microbial communities across host evolutionary history PLOS Biology (open access) By Brooks AW*, Kohl KD*, Brucker RM*, van Opstal EJ, Bordenstein SR (Co-first authors) Select coverage:
Description: Studies on the assembly and function of host-microbiota symbioses are inherently complicated by the diverse effects of diet, age, sex, host genetics, and endosymbionts. Central to unraveling one effect from the other is an experimental framework that reduces confounders. Using common rearing conditions across four animal groups (deer mice, flies, mosquitoes, and wasps) that span recent host speciation events to more distantly related host genera, this study tests whether microbial community assembly is generally random with respect to host relatedness or "phylosymbiotic," in which the phylogeny of the host group is congruent with ecological relationships of their microbial communities. Across all four animal groups and one external dataset of great apes, we demonstrate phylosymbiosis to varying degrees in each group. Moreover, consistent with selection on host–microbiota or holobiont interactions driving phylosymbiosis, transplanting interspecific microbial communities in mice significantly decreased their ability to digest food. Similarly, wasps that received transplants of microbial communities from different wasp species had lower survival than those given their own microbiota. Overall, this experimental and statistical framework shows how microbial community assembly and functionality across related species can be linked to animal evolution, health, and survival.