Extremely reduced supergroup F Wolbachia: transition to obligate insect symbionts

Abstract

Background Wolbachia belong to highly abundant bacteria which are frequently found in invertebrate microbiomes and manifest by a broad spectrum of lifestyles from parasitism to mutualism. Wolbachia Supergroup F is a particularly interesting group as it gave rise to symbionts of both arthropods and nematodes, and some of its members are obligate mutualists. Investigations on evolutionary transitions among the different symbiotic stages have been hampered by a lack of the known diversity and genomic data for the supergroup F members. Results Based on amplicon screening, short and long read WGS approaches, and laser confocal microscopy, we characterize five new supergroup F Wolbachia strains from four chewing lice species. These strains reached different evolutionary stages and represent two remarkably different types of symbiont genomes. Three of the genomes resemble other known members of Wolbachia F supergroup, while other two show typical signs of ongoing gene inactivation and removal (genome size, coding density, low number of pseudogenes). Particularly, wMeur1, a symbiont fixed in microbiomes of Menacanthus eurysternus across four continents, possesses a highly reduced genome of 733,850 bp. The horizontally acquired capacity for pantothenate synthesis and localization in specialized bacteriocytes suggest its obligate nutritional role. Conclusions The genome of wMeur1 strain, from the M. eurysternus micobiome, represents the smallest currently known Wolbachia genome and the first example of Wolbachia which has completed genomic streamlining as known from the gammaproteobacterial obligate symbionts. This points out that despite the large amount and great diversity of the known Wolbachia strains, evolutionary potential of these bacteria still remains underexplored. The diversity of the four chewing lice microbiomes indicates that this vast parasitic group may provide suitable models for further investigations.

A highly divergent Wolbachia with a tiny genome in an insect-parasitic tylenchid nematode

“…While the genomes of facultative Wolbachia symbionts of arthropods, such as strains that cause cytoplasmic incompatibility, lie in the range of approximately 1–1.5 Mb, genomes of obligate Wolbachia symbionts of filarial nematodes are smaller, ranging from 860 kb to approximately 1.1 Mb. Up to now, the smallest reported Wolbachia genome, described in a recent preprint, is that of a symbiont of Menacanthus chewing lice, within Wolbachia supergroup F, a group that includes symbionts of other blood-feeding insects and some filarial nematodes, at approximately 733 kbp [55]. Another common feature of obligate symbionts is loss of genes involved in DNA replication, repair and recombination, which is thought to drive incredibly rapid rates of substitution [39,56,57].…”

“…Despite being so highly divergent, the w How genome is a complete subset of all other Wolbachia , unlike the reduced genome Wolbachia in Menacanthus chewing lice, for example, which has horizontally acquired genes involved in panthotenate synthesis [55]. Interestingly, while w How has lost a huge number of genes, it has retained some, but not all, pathways that are also found in filarial nematode symbionts, which have been independently colonized at least three times by different lineages of Wolbachia [25], all of which have converged on a similar complement of genes.…”

Metagenomics of culture isolates and insect tissue illuminate the evolution of Wolbachia, Rickettsia and Bartonella symbionts in Ctenocephalides spp. fleas

“…Both w Cori and w CfeT contained the genes panB , panC , panD and panG , which are related to pantothenate biosynthesis. These genes, except panD , have only previously been reported in the Wolbachia endosymbiont of Menacanthus eurysternus ( w Meur1), a supergroup F strain with a highly reduced genome [91]. As mentioned above, the pantothenate biosynthesis island was found in the EAM region of WOCori2 prophage (), suggesting a possible role of phages in the LGT of these genes.…”

“…The C. felis genome contains laterally transferred, CI-like antidote genes that could potentially neutralize Wolbachia -induced CI [34]; hence, determining if this is also true for C. orientis will be important to further our understanding of flea –Wolbachia relationships. The presence of pantothenate biosynthesis genes in these supergroup I genomes, which are otherwise very sparsely distributed in the accessory genome of Wolbachia [91], adds further complexity to the potential host–symbiont phenotypes mediated by w CfeT and w Cori. This may indicate that vitamin provisioning is important in the symbiosis of Ctenocephalides spp.…”

“…Historically, the classification of Wolbachia phenotypes was shaped by comparison between the reproductive parasitism and evidence of horizontal transmission in supergroups A and B, and the apparent obligate mutualism and host–symbiont coevolution exhibited by the filarial nematode-specific clades C and D [112]. Although it is now known that Wolbachia co-evolution with filariae has broken down on multiple occasions, with numerous examples of symbiont loss and gain [113], evidence of co-evolution between Wolbachia and its hosts in some haematophagous arthropod taxa has provided new impetus to research on mutualistic relationships involving Wolbachia [91, 114, 115]. The best studied of these is the symbiosis between the bedbug C. lectularius and Wolbachia strain wCle from supergroup F, which is housed in a bacteriocyte and provisions riboflavin and biotin (deficient in blood diets), the latter via the BOOM [38].…”