Multiple origins of nematode-Wolbachiasymbiosis in supergroup F and convergent loss of bacterioferritin in filarialWolbachia

The intracellular endosymbiotic proteobacteria Wolbachia have evolved across the phyla nematoda and arthropoda. In Wolbachia phylogeny, supergroup F is the only clade known so far with members from both arthropod and filarial nematode hosts and therefore can provide unique insights into their evolution and biology. In this study, 4 new supergroup F Wolbachia genomes have been assembled using a metagenomic assembly and binning approach, w Moz and w Mpe from the human filarial parasites Mansonella ozzardi and Mansonella perstans , and w Ocae and w MoviF from the blue mason bee Osmia caerulescens and the sheep ked Melophagus ovinus respectively. A comprehensive phylogenomic analysis revealed two independent origins of filarial Wolbachia in supergroup F, most likely from ancestral arthropod hosts. The analysis also reveals that the switch from arthropod to filarial host is accompanied by a convergent pseudogenization and loss of the bacterioferritin gene, a phenomenon found to be shared by all filarial Wolbachia , even those outside supergroup F. These observations indicate that differences in heme metabolism might be a key feature distinguishing filarial and arthropod Wolbachia . The new genomes provide a valuable resource for further studies on symbiosis, evolution, and the discovery of new antibiotics to treat mansonellosis. Significance statement Wolbachia are bacterial endosymbionts of medically important parasitic filarial nematodes and arthropods. The evolutionary history and biological roles of Wolbachia in these different hosts are not well understood. The supergroup F in Wolbachia phylogeny harbors members from both filarial and arthropod hosts, providing an unparalleled opportunity for genomic comparisons to uncover distinguishing characteristics. This study provides new genomes from filarial and arthropod Wolbachia from this unique supergroup. Their phylogenomic analysis reveals multiple, independent transfers of Wolbachia from arthropod to filariae. Remarkably, these transfers were associated with a convergent loss of the bacterioferritin gene, a key regulator of heme metabolism. Heme supplementation is considered a critical component of Wolbachia - filaria symbiosis. We demonstrate bacterioferritin loss is a novel feature exclusive to filarial Wolbachia .