CRISPR-resolved virus-host interactions in a municipal landfill include non-specific viruses, hyper-targeted viral...

Viruses are the most abundant microbial guild on the planet, impacting microbial community structure and ecosystem services. Viruses are specifically understudied in engineered environments, including examinations of their host interactions. We examined host-virus interactions via host CRISPR spacer to viral protospacer mapping in a municipal landfill across two years. Viruses comprised ~ 4% of both the unassembled reads and assembled basepairs. A total of 458 unique virus-host connections captured hyper-targeted viral populations and host CRISPR array adaptation over time. Four viruses were predicted to infect across multiple phyla, suggesting that some viruses are far less host-specific than is currently understood. We detected 161 viral elements that encode CRISPR arrays, including one with 187 spacers, the longest virally-encoded CRISPR array described to date. Virally-encoded CRISPR arrays targeted other viral elements in interviral conflicts. CRISPR-encoding proviruses integrated into host chromosomes were latent examples of CRISPR-immunity-based superinfection exclusion. The bulk of the observed virus-host interactions fit the one-virus-one-host paradigm, but with limited geographic specificity. Our networks highlight rare and previously undescribed complex interactions influencing the ecology of this dynamic engineered system. Our observations indicate landfills, as heterogeneous contaminated sites with unique selective pressures, are key locations for atypical virus-host dynamics.