Fur microbiome as a putative source of symbiotic bacteria in sucking lice.

Symbiosis between insects and bacteria has been established countless times. While it is well known that the symbionts originated from a variety of different bacterial taxa, it is usually difficult to determine their environmental source and a route of their acquisition by the host. In this study, we address this question using a model of Neisseriaceae symbionts in rodent lice. These bacteria established their symbiosis independently with different louse taxa (Polyplax, Hoplopleura, Neohaematopinus), most likely from the same environmental source. We first applied amplicon analysis to screen for candidate source bacterium in the louse environment. Since lice are permanent ectoparasites, often specific to the particular host, we screened various microbiomes associated with three rodent species (Microtus arvalis, Clethrionomys glareolus, and Apodemus flavicollis). The analyzed samples included fur, skin, spleen, and other ectoparasites sampled from these rodents. The fur microbiome data revealed a Neisseriaceae bacterium, closely related to the known louse symbionts. The draft genomes of the environmental Neisseriaceae, assembled from all three rodent hosts, converged to a remarkably small size of approximately 1.4 Mbp, being even smaller than the genomes of the related symbionts. Our results suggest that the rodent fur microbiome can serve as a source for independent establishment of bacterial symbiosis in associated louse species. We further propose a hypothetical scenario of the genome evolution during the transition of a free-living bacterium to the member of the rodent fur-associated microbiome and subsequently to the facultative and obligate louse symbionts.

Arsenophonus symbiosis with louse flies: multiple origins, coevolutionary dynamics, and metabolic significance.

IMPORTANCE: Insects that live exclusively on vertebrate blood utilize symbiotic bacteria as a source of essential compounds, e.g., B vitamins. In louse flies, the most frequent symbiont originated in genus Arsenophonus, known from a wide range of insects. Here, we analyze genomic traits, phylogenetic origins, and metabolic capacities of 11 Arsenophonus strains associated with louse flies. We show that in louse flies, Arsenophonus established symbiosis in at least four independent events, reaching different stages of symbiogenesis. This allowed for comparative genomic analysis, including convergence of metabolic capacities. The significance of the results is twofold. First, based on a comparison of independently originated Arsenophonus symbioses, it determines the importance of individual B vitamins for the insect host. This expands our theoretical insight into insect-bacteria symbiosis. The second outcome is of methodological significance. We show that the comparative approach reveals artifacts that would be difficult to identify based on a single-genome analysis.