Diverse viruses infect nitrifying archaea and bacteria communities in soil

Abstract

Soil virus communities are diverse and dynamic but contributions to specific processes, such as nitrification, are largely uncharacterised. Chemolithoautotrophic nitrifiers perform this essential component of the nitrogen cycle and are established model groups for linking phylogeny, evolution and ecophysiology due to limited taxonomic and functional diversity. Ammonia-oxidising bacteria (AOB) dominate the first step of ammonia oxidation at high supply rates, with ammonia-oxidising archaea (AOA) and complete ammonia-oxidising Nitrospira (comammox) often active at lower supply rates or when AOB are inactive, and nitrite-oxidising bacteria (NOB) completing canonical nitrification. Here, the diversity and genome content of dsDNA viruses infecting different nitrifier groups were characterised after in situ enrichment via differential host inhibition, a selective approach that alleviates competition for non-inhibited populations to determine relative activity. Microcosms were incubated with urea to stimulate nitrification and amended with 1-octyne or 3,4-dimethylpyrazole phosphate (AOB inhibited), acetylene (all ammonia oxidisers inhibited), or no inhibitor (AOB stimulated), and virus-targeted metagenomes characterised using databases of host genomes, reference (pro)viruses and hallmark genes. Increases in the relative abundance of nitrifier host groups were consistent with predicted inhibition profiles and concomitant with increases in the relative abundance of their viruses, represented by 200 viral operational taxonomic units. These included 61 high-quality/complete virus genomes 35-173 kb in length and possessing minimal similarity to validated families. Most AOA viruses were placed within a unique lineage and viromes were enriched in AOA multicopper oxidase genes. These findings demonstrate that focussed incubation studies facilitate characterisation of host-virus interactions associated with specific functional processes.