Abstract
Terrestrial arthropods are commonly infected with maternally inherited bacterial symbionts that cause cytoplasmic incompatibility (CI). In CI, the outcome of crosses between symbiont-infected males and uninfected females is reproductive failure, increasing the relative fitness of infected females and leading to spread of the symbiont in the host population. CI symbionts have profound impacts on host genetic structure and ecology and may lead to speciation and the rapid evolution of sex determination systems. Cardinium hertigii, a member of the Bacteroidetes and symbiont of the parasitic wasp Encarsia pergandiella, is the only known bacterium other than the Alphaproteobacteria Wolbachia to cause CI. Here we report the genome sequence of Cardinium hertigii cEper1. Comparison with the genomes of CI–inducing Wolbachia pipientis strains wMel, wRi, and wPip provides a unique opportunity to pinpoint shared proteins mediating host cell interaction, including some candidate proteins for CI that have not previously been investigated. The genome of Cardinium lacks all major biosynthetic pathways but harbors a complete biotin biosynthesis pathway, suggesting a potential role for Cardinium in host nutrition. Cardinium lacks known protein secretion systems but encodes a putative phage-derived secretion system distantly related to the antifeeding prophage of the entomopathogen Serratia entomophila. Lastly, while Cardinium and Wolbachia genomes show only a functional overlap of proteins, they show no evidence of laterally transferred elements that would suggest common ancestry of CI in both lineages. Instead, comparative genomics suggests an independent evolution of CI in Cardinium and Wolbachia and provides a novel context for understanding the mechanistic basis of CI.
Highlights
Bacterial symbionts of terrestrial arthropods are common, influential associates, known to affect fundamental aspects of the host life history, ecology, and evolution
Many arthropods are infected with bacterial symbionts that are maternally transmitted and have a great impact on their hosts’ biology, ecology, and evolution
One of the most common phenotypes of facultative symbionts appears to be cytoplasmic incompatibility (CI), a type of reproductive failure in which bacteria in males modify sperm in a way that reduces the reproductive success of uninfected female mates
Summary
Bacterial symbionts of terrestrial arthropods are common, influential associates, known to affect fundamental aspects of the host life history, ecology, and evolution. These maternally inherited bacteria may, for example, provide essential nutrients supplementing their host’s diet, confer protection against natural enemies, increase stress resistance, or influence host plant suitability [1,2,3,4]. Others have evolved sophisticated means of manipulating the arthropod host’s reproduction in ways that cause the symbiont to spread within the host population [5,6]. The symbiont spreads because of the decreased fitness of uninfected relative to infected female hosts [5]. In the fertilized oocyte of an incompatible mating of Drosophila or the parasitic wasp Nasonia vitripennis, CI Wolbachia leads to asynchrony of the timing of maternal and paternal chromosome condensation and segregation during the first embryonic mitotic division, disrupting
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