Metagenomics reveals potential interactions between Patescibacteriota and their phages in groundwater ecosystems.

UNLABELLED: Patescibacteriota is a vast lineage composed of bacteria with ultra-small size, streamlined genomes, notable defects in core metabolic potential, and symbiotic lifestyle, which are widely detected in groundwater ecosystems. Increasing attention has focused on the physiological and ecological significance of Patescibacteriota, while the potential interactions between Patescibacteriota and their phages still need more exploration. Here, we collected 82 groundwater metagenomic data sets and further derived 1,162 phages with the potential to infect 2,439 groundwater Patescibacteriota metagenome-assembled genomes (MAGs). Notably, the groundwater Patescibacteriota MAGs were predominantly infected by temperate phages, and viral operational taxonomic unit/host Patescibacteriota operational taxonomic unit (OTU) abundance ratios were significantly negatively correlated with the relative abundance of host Patescibacteriota OTUs. Intriguingly, the groundwater Patescibacteriota phages encoded various auxiliary metabolic genes (AMGs) that might promote symbiotic lifestyle and metabolic potential of host Patescibacteriota MAGs. These included AMGs associated with concanavalin A-like lectin/glucanases superfamily and O-Antigen nucleotide sugar biosynthesis, which could enhance surface adhesion of host Patescibacteriota MAGs. Moreover, AMGs related to the ABC transport system and the P-type transporter could strengthen metabolic exchange and uptake of essential nutrients from the surroundings. Additionally, AMGs involved in various metabolic pathways might alleviate metabolic deficiencies in host Patescibacteriota MAGs.

IMPORTANCE: Here, we sought phages that were capable of infecting Patescibacteriota metagenome-assembled genomes (MAGs), and further explored the diversity and novelty of Patescibacteriota phages, as well as the mechanisms underlying phage-Patescibacteriota interactions in groundwater ecosystems. The abundance profiles of phage-Patescibacteriota interactions suggested that lysogenic infection may represent a mutually adapted strategy between Patescibacteriota and their phages in groundwater ecosystems. Furthermore, the groundwater Patescibacteriota phages possessed diverse auxiliary metabolic genes which might facilitate the symbiotic associations and metabolic exchange between host Patescibacteriota MAGs and other free-living microbes and expand the metabolic capabilities of host Patescibacteriota MAGs. This study elucidated the mechanisms of phage-Patescibacteriota interactions and the potential roles of phages in modulating the physiology and ecology of Patescibacteriota within groundwater ecosystems.