Abstract
Wolbachia, one of the most widespread endosymbionts, is a target for biological control of mosquito-borne diseases (malaria and dengue virus), and antibiotic elimination of infectious filarial nematodes. We sequenced and analyzed the genome of a new Wolbachia strain (wPpe) in the plant-parasitic nematode Pratylenchus penetrans. Phylogenomic analyses placed wPpe as the earliest diverging Wolbachia, suggesting two evolutionary invasions into nematodes. The next branches comprised strains in sap-feeding insects, suggesting Wolbachia may have first evolved as a nutritional mutualist. Genome size, protein content, %GC, and repetitive DNA allied wPpe with mutualistic Wolbachia, whereas gene repertoire analyses placed it between parasite (A, B) and mutualist (C, D, F) groups. Conservation of iron metabolism genes across Wolbachia suggests iron homeostasis as a potential factor in its success. This study enhances our understanding of this globally pandemic endosymbiont, highlighting genetic patterns associated with host changes. Combined with future work on this strain, these genomic data could help provide potential new targets for plant-parasitic nematode control.
Highlights
Wolbachia pipientis is the most common bacterial endosymbiont of arthropods, occurring in 61–66% of insect species[1,2,3,4], yet its evolution is still not well understood
We applied fluorescence in situ hybridization (FISH) confocal microscopy to confirm the presence of Wolbachia cells in P. penetrans
Ribosomal rRNA 16S similarity and presence of homologs to all Wolbachia marker genes clearly place this bacteria from P. penetrans within the genus Wolbachia[49,50,51], while phylogenomic results placed it at the base of the tree, suggesting that plant-parasitic nematodes were the first hosts for Wolbachia
Summary
Wolbachia pipientis (alphaproteobacteria) is the most common bacterial endosymbiont of arthropods, occurring in 61–66% of insect species[1,2,3,4], yet its evolution is still not well understood. Wolbachia research has recently flourished with a growing set of genomic and transcriptomic contributions[16,24,25,26,27,28], permitting a view of both phylogenomic relationships and genotype-to-phenotype hypotheses[7,29,30] These analyses show that most known Wolbachia strains fall into two major sister groups. The second group is largely comprised of obligate mutualists, dominated by filarial nematode hosts, long evolutionary distances, with more limited host-switching, genetic exchange, and co-infections (supergroups C, D, and F)[18,31,32,33]. Until the present study phylogenomic analyses including plant-parasitic nematode-associated Wolbachia were not possible, since genomic data was lacking[37,40]
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