Huge and variable diversity of episymbiotic CPR bacteria and DPANN archaea in groundwater ecosystems

Abstract

Candidate Phyla Radiation (CPR) bacteria and DPANN archaea are uncultivated, small-celled symbionts often detected in groundwater. However, variations in CPR/DPANN organism abundance, distribution, taxonomic diversity, and degree/nature of host association with groundwater chemistry remain understudied. Here, we performed genome-resolved metagenomic characterization of one agriculturally-impacted and seven pristine groundwater microbial communities in California, recovering 746 dereplicated CPR and DPANN genomes. Our finding of up to 31% CPR bacteria and 4% DPANN archaea in the pristine sites, which serve as local sources of drinking water, may hold health relevance, given growing awareness of the presence of CPR/DPANN organisms in human microbiomes and their association with disease. There is little species-level genome overlap across groundwater sites, indicating that CPR and DPANN communities are highly differentiated according to host populations and physicochemical conditions. Cryo-TEM imaging and genomic analyses indicate that CPR growth may be stimulated by attachment to the surface of host cells, and identified CPR and DPANN lineages with particularly prevalent and/or resilient host cell attachment. These results establish the huge but site-specific diversity of CPR bacteria and DPANN archaea coexisting with diverse hosts in groundwater aquifers, and raise important questions about potential impacts on human health.