Effect of clay mineral on bacteria–virus interactions and the fate of microbial biomass carbon

Abstract

Viruses are the major drivers of global geochemical cycles through lysis of host bacteria. The release of cellular organic matter (OM) to the environment via viral lysis short-circuits the carbon flow from bacteria to higher trophic levels, a process known as the “viral shunt”. However, current understanding of bacteria–virus interactions is limited to the oceans. In sediments and soils, clay minerals are ubiquitous, but their roles in controlling viral lysis of host bacteria are virtually unknown. Here, we established a model experimental system using clay mineral montmorillonite, a common bacterium Shewanella oneidensis MR-1, and its lytic virus MSO-5 to investigate the impacts of clay mineral on bacteria–virus interactions, as well as the fate of the released OM. X-Ray Diffraction (XRD) and pyrolysis gas chromatography-mass spectrum (PY-GC–MS) were used to detect OM intercalation into montmorillonite interlayer. The results showed that the presence of montmorillonite delayed lysis of bacterial host due to its spatial separation from virus and delayed release of dissolved organic matter (DOM) through adsorption. Low molecular weight compounds released from virus-induced cell lysis, mainly benzene derivatives, N-containing compounds, and ketones were preferentially intercalated into the interlayer space of montmorillonite. Our results demonstrate that clay minerals play an important role in bacteria–virus interactions in controlling release and preservation of microbially-derived organic matter, which is expected to have an increasingly important impact on carbon cycling as sediment inflow increases with global warming. This study advances our understanding of mineral–bacteria–virus interactions in the viral shunt, especially in clay-rich environments such as soils and sediments.