Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics study

The dynamics of the structure of polyhydroxyalkanoate-producing mixed microbial cultures (PHA-MMCs) during enrichment and maintenance is an unsolved problem. The effect of phages has been proposed as a cause of dynamic changes in community structure, but evidence is lacking. To address this question, five PHA-MMCs were enriched, and biological samples were sampled temporally to study the interactions between phage and bacterial members by combining metagenomics and metatranscriptomics. A total of 963 metagenome-assembled genomes (MAGs) and 4,294 phage operational taxonomic units (pOTUs) were assembled from bulk metagenomic data. The dynamic changes in the structure of phage and bacterial communities were remarkably consistent. Structural equation modeling analysis showed that phages could infect and lyse dominant species to vacate ecological niches for other species, resulting in a community succession state in which dominant species alternated. Seven key auxiliary metabolic genes (AMGs), <i>phaC</i>, <i>fadJ</i>, <i>acs</i>, <i>ackA</i>, <i>phbB</i>, <i>acdAB,</i> and <i>fadD</i>, potentially contributing to PHA synthesis were identified from phage sequences. Importantly, these AMGs were transcribed, indicating that they were in an active expression state. The meta-analysis provides the first catalog of phages in PHA-MMCs and the AMGs they carry, as well as how they affect the dynamic changes in bacterial communities. This study provides a reference for subsequent studies on understanding and regulating the microbial community structure of open microbial systems.IMPORTANCEThe synthesis of biodegradable plastic PHA from organic waste through mixed microbial cultures (PHA-MMCs), at extremely low cost, has the potential for expanded production. However, the dynamics of dominant species in PHA-MMCs are poorly understood. Our results demonstrate for the first time the impact of phages on the structure of bacterial communities in the PHA-MMCs. There are complex interactions between the PHA producers (e.g., <i>Azomonas</i>, <i>Paracoccus</i>, and <i>Thauera</i>) and phages (e.g., Casadabanvirus and unclassified Hendrixvirinae). Phage communities can regulate the activity and structure of bacterial communities. In addition, the AMGs related to PHA synthesis may hitchhike during phage-host infection cycles, enabling their dissemination across bacterial communities, and phages may act as a critical genetic reservoir for bacterial members, facilitating access to PHA synthesis-related functional traits. This study highlights the impact of phages on bacterial community structure, suggesting that phages have the potential to be used as a tool for better controlling the microbial community structure of PHA-MMCs.