Comparative genomics of Wolbachia-Cardinium dual endosymbiosis in a plant-parasitic nematode

Authors: BROWN, A - Texas Tech University; WASALA, S - Oregon State University; HOWE, D - Oregon State University; Peetz, Amy; Zasada, Inga; DENVER, D - Oregon State University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/28/2018
Publication Date: 10/16/2018
Citation: Brown, A.M., Wasala, S.K., Howe, D.K., Peetz, A.B., Zasada, I.A., Denver, D.R. 2018. Comparative genomics of Wolbachia-Cardinium dual endosymbiosis in a plant-parasitic nematode. Frontiers in Microbiology. 9:2482. https://doi.org/10.3389/fmicb.2018.02482.
DOI: https://doi.org/10.3389/fmicb.2018.02482

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 dual infection of the root lesion nematode by the endosymbionts Cardinium and Wolbachia. The DNA of Wolbachia and Cardinium was extracted and sequenced and then the potential ways that these endosymbionts interact with their nematode host were considered by analyzing the DNA sequences. Presence of Wolbachia and Cardinium in the nematode was also determined using fluorescent probes. This research was the first to report a dual endosymbiotic relationship in a nematode. It was also discovered that the endosymbionts were dispersed throughout the nematode's body. These results are significant because they provide a framework for further understanding the evolution and function of Cardinium and Wolbachia in their hosts. This research will be used by scientists to continue to explore the role of the endosymbionts in host function and may lead to the development of novel management methods to minimize the impact of plant-parasitic nematodes on agriculture.

Technical Abstract: Wolbachia and Cardinium are among the most important and widespread of all endosymbionts, occurring in nematodes and more than half of insect and arachnid species, sometimes as coinfections. These symbionts are of significant interest as potential agents of artificial and natural biocontrol due to their abilities to cause major effects on host biology and reproduction through cytoplasmic incompatibility, sex ratio distortion, or obligate mutualism. The ecological and metabolic effects of coinfections are not well understood. This study examined a Wolbachia-Cardinium coinfection in the plant-parasitic nematode, Pratylenchus penetrans, producing the first detailed study of such a coinfection using fluorescence in situ hybridization (FISH), genome sequencing, and comparative genomics. Results from FISH and single-nematode PCR showed most individuals in a focal population carried Cardinium (denoted strain cPpe), while 48% were also co-infected with Wolbachia (denoted strain wPpe). Both endosymbionts showed dispersed tissue distribution with highest densities in the anterior intestinal walls and gonads. Phylogenomic analyses confirmed an early place of cPpe and long distance from a sister strain in another plant-parasitic nematode, Heterodera glycines, supporting a long history of both Cardinium and Wolbachia in plant-parasitic nematodes. Genome features showed cPpe was missing a plasmid and biotin and lipoate synthetic capacity present in other strains, despite having a slightly larger genome. The larger genome revealed expansions of gene families likely involved in host-cellular interactions, and more than 2% of the genes of cPpe and wPpe were identified as candidate horizontally transferred genes, with some of these from eukaryotes, including nematodes. A model of the possible Wolbachia-Cardinium interaction is proposed.