A hydrocarbon-contaminated aquifer reveals a Piggyback-the-Persistent viral strategy

Subsurface environments hold the largest reservoir of microbes in the biosphere. They play essential roles in transforming nutrients, degrading contaminants and recycling organic matter. Here, we propose a previously unrecognised fundamental microbial process that influences aquifer bioremediation dynamics and that applies to all microbial communities. In contrast to previous models, our proposed Piggyback-the-Persistent (PtP) mechanism occurs when viruses become more dominated by those exhibiting temperate rather than lytic lifestyles driven by persistent chemicals (in our case chlorinated-hydrocarbon pollutants) that provide long-term carbon sources and that refocus the aquifer carbon cycle, thus altering the microbial community. In this ultra-oligotrophic system, the virus:microbial ratio (VMR) ranges from below the detection limit of 0.0001 to 0.6, well below the common aquatic range of 3-10. Shortest-average-path network analysis revealed VMR and trichlorethene (TCE) as nodes through which ecosystem information and biomass most efficiently pass. Novel network rearrangement revealed a hierarchy of Kill-the-Winner (KtW), Piggyback-the-Winner (PtW) and PtP nodes. We propose that KtW, PtW and PtP occur simultaneously as competing strategies, with their relative importance depending on conditions at a particular time and location with unusual nutrient sources, such as TCE, appearing to contribute to a shift in this balance between viral mechanisms.