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Title: Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts

item BROWN, A - Oregon State University
item WASALA, S - Oregon State University
item HOWE, D - Oregon State University
item Peetz, Amy
item Zasada, Inga
item DENVER, D - Oregon State University

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/21/2016
Publication Date: 10/13/2016
Citation: Brown, A.M., Wasala, S.K., Howe, D.K., Peetz, A.B., Zasada, I.A., Denver, D. 2016. Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts. Scientific Reports. 6(34955). doi:10.1038/srep34955.

Interpretive Summary: Plant-parasitic nematodes are microscopic worms that cause 100 billion dollars in global crop losses annually. Ways to manage these production-limiting pests are becoming fewer and more regulated. There is a need to discovery new ways to manage plant-parasitic nematodes. Endosymbionts, microbes that live within a host, have been shown to be targets for the management of insects and nematode parasites of humans. The focus of this research was the nematode endosymbiont Wolbachia. The DNA of Wolbachia was extracted and sequenced and then the relationship of this Wolbachia from a plant-parasitic nematode was compared to other Wolbachia that are found in insects and other nematodes. This research was the first to report a Wolbachia endosymbiont in the root lesion nematode. It was also discovered that plant-parasitic nematodes were the first hosts for Wolbachia, not insects as previously thought. These results are significant because they provide a framework for further understanding the evolution of Wolbachia in their hosts. This research will be used by scientists to continue to explore the role of the endosymbiont Wolbachia in host function and may lead to the development of novel management methods targeting Wolbachia to minimize the impact of plant-parasitic nematodes on agriculture.

Technical Abstract: Wolbachia, the most widely studied endosymbiont in arthropods, 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 strain (wPpe) in the plant-parasitic nematode Pratylenchus penetrans. Phylogenomic analyses robustly 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 transitions between hosts, and raises interest in Wolbachia for plant-parasitic nematode management.