Can a necromenic nematode serve as a biological Trojan horse for an invasive ant?

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Alice Hotopp, School of Ecology and Environmental Sciences, University of Maine, Orono, ME, Samantha Silverbrand, School of Marine Sciences, University of Maine, Orono, ME, Suzanne L. Ishaq, School of Food and Agriculture, University of Maine, Orono, ME, Jonathan E. Dumont, College of Science and Humanities, Husson University, Bangor, ME, Amy Michaud, Department of Entomology & Nematology, University of California, Davis, Davis, CA, Jean MacRae, Department of Civil and Environmental Engineering, University of Maine, Orono, ME, S. Patricia Stock, School of Animal and Comparative Biomedical Sciences, University of Arizona, Tuscon, AZ and Eleanor Groden, School of Biology and Ecology, University of Maine, Orono, ME

Background/Question/Methods
The invasive European fire ant (Myrmica rubra) threatens native ant species and human health along the coast of Maine, United States. M. rubra mortality has been associated with infection by Pristionchus entomophagus, a necromenic nematode that is hypothesized to transfer pathogenic bacteria acquired from the environment to ant colonies. To investigate this hypothesis, we conducted a series of experiments on nematode-infected ants collected from Mount Desert Island. First, we isolated bacteria cultured from nematodes emerging from M. rubra cadavers and assessed the ability of the nematodes to acquire and transfer environmental bacteria to Galleria mellonella waxworm larvae. Second, we identified bacteria which were potentially transferred from nematodes to infected ant nests on MDI using bacterial community similarity and sequence tracking methods.
Results/Conclusions
Multiple bacterial species, including Paenibacillus spp., were found in the nematodes’ digestive tract. Serratia marcescens, Serratia nematodiphila, and Pseudomonas fluorescens were collected from the hemolymph of nematode-infected G. mellonella larvae. Variability was observed in insect virulence in relation to the site origin of the nematodes. In vitro assays confirmed uptake of red fluorescence protein (RFP)-labeled Pseudomonas aeruginosa strain PA14 by nematodes. Bacteria were highly concentrated in the digestive tract of adult nematodes, some bacteria were observed in the digestive tract of juveniles with a more significant amount on their cuticle, and none on the cuticle of adults. RFP-labeled P. aeruginosa were not observed in hemolymph of G. mellonella larvae, indicating an apparent lack of bacterial transfer from juvenile nematodes to the insects despite larval mortality.
Host species was the primary factor affecting bacterial community profiles. Spiroplasma sp. and Serratia marcescens sequences were shared across ants, nematodes, and nematode-exposed G. mellonella larvae. Alternative to the idea of transferring bacteria from environment to host, we considered whether nematode-exposure might disorder or depauperate the endobiotic community of an insect host. While total bacterial diversity was not statistically lower in nematode-exposed G. mellonella larvae when compared to controls, 16 bacterial sequence variants were less abundant in nematode-exposed larvae, while three were increased, including Serratia, Pseudomonas, and Proteus.
This study suggests that transfer of bacteria from nematodes to ants is feasible, although largely serendipitous, and may contribute to ant mortality in Maine. Hypothetically, the use of an engineered biological control, such as nematodes carrying specifically-seeded bacterial species, may be effective, especially if the pathogenic bacteria are naturally found in soil ecosystems and represent a low risk for biosafety control.