Wolbachia springs eternal: symbiosis in Collembola is associated with host ecology

Abstract

Wolbachia are endosymbiotic alpha-proteobacteria infecting a wide range of arthropods and nematode hosts with diverse interactions, from reproductive parasites to obligate mutualists. Their taxonomy is defined by lineages called supergroups (labelled by letters of the alphabet), while their evolutionary history is complex, with multiple horizontal transfers and secondary losses. One of the least recently derived, supergroup E, infects springtails (Collembola), widely distributed hexapods, with sexual and/or parthenogenetic populations depending on species. To better characterize the diversity of Wolbachia infecting springtails, the presence of Wolbachia was screened in 58 species. Eleven (20%) species were found to be positive, with three Wolbachia genotypes identified for the first time in supergroup A. The novel genotypes infect springtails ecologically and biologically different from those infected by supergroup E. To root the Wolbachia phylogeny, rather than distant other Rickettsiales, supergroup L infecting plant-parasitic nematodes was used here. We hypothesize that the ancestor of Wolbachia was consumed by soil-dwelling nematodes, and was transferred horizontally via plants into aphids, which then infected edaphic arthropods (e.g. springtails and oribatid mites) before expanding into most clades of terrestrial arthropods and filarial nematodes.

No evidence for phylogenetic structure or environmental filtering of springtail microbiomes

“…2021). Interestingly, we could not detect a recently reported phylogenetic signal in Wolbachia infections in springtails (Rodrigues et al . 2023), despite the identification of several Wolbachia strains in the sequence data (Supp.…”

“…Although we were able to detect several strains of Wolbachia (Supp. Table 2), we could not confirm recently reported phylogenetic signals in Wolbachia infections in springtails (Rodrigues et al . 2023).…”

Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia

“…Unfortunately, we did not recover the 16S rRNA sequence from w Paga, but its position on a long branch is consistent with that of a previous reported symbiont from Leptotrombidium scutellare in Japan [ 16 ]. It has been hypothesized that Wolbachia evolved in the soil milieu [ 59 ] through associations with parasitic nematodes of plants (supergroup L [ 60 ]) or saprotrophic flies (W [ 61 ]), and may have been horizontally transmitted via plants, honeydew, and/or insect carcasses to other hosts of early-branching Wolbachia clades including the banana aphid (M), springtails (E), oribatid mites (E), and fleas (I) – the latter being detritivorous in the larval stage. In accordance with this model, the free-living lifecycle of trombiculid mites proceeds underground, where the nymphal and adult stages predate small edaphic arthropods or their eggs.…”