Nematode hitchhiking in soil bacteriophage dispersal

Lytic bacteriophages are major drivers of bacterial mortality and biogeochemical cycles in several ecosystems, roles that have also been hypothesized in soil. Phage particles have no metabolism of their own, yet to achieve sustainable replication they must travel from one host to the next through the surrounding environment. Evidence from soil physics and phage biology suggests that this is a hazardous journey for unprotected phages, especially under the prevailing assumption that dispersal occurs by diffusion. However, many other viruses overcome dispersal challenges by taking advantage of vectors – third-party organisms that carry the virus from one host to the next. We hypothesized that bacterivorous nematodes play this role in soil, picking up phages while feeding on bacteria and transferring them to uninfected bacteria while foraging. We postulated that nematodes would provide active and directed transport of phages between bacterial patches via two possible mechanisms. First, nematode intestines could temporarily harbour infected bacteria during nematode movement. Second, nematodes could carry phages through external attachment to the nematode cuticle. Using experiments with model nematodes (C. elegans) and bacteria (E. coli, P. putida) along with phages (T7, Phi Ppu-W11) we confirmed that transfer occurs at high frequency when facilitated by nematodes, and does not occur without nematodes. Resource availability was found to influence the transfer by modulating nematode behaviour in agar, but this effect was not found in structured compost habitats. Based on these results we propose that vectors are crucial for soil phage dispersal, suggesting that phage roles in soil function are mediated by interactions with local fauna.