The phylogenetic and global distribution of extracellular bioplastic degrading genes

Polyhydroxyalkanoates (PHAs) are a family of microbially-made polyesters commercialized as biodegradable plastics. PHA production rates are predicted to increase as concerns around environmental plastic contamination and limited fossil fuel resources have increased the importance of biodegradable and bio-based plastic alternatives. Microbially-produced PHA depolymerases are the key enzymes mediating PHA biodegradation, but only a few PHA depolymerases have been well-characterized and screens employing metagenomic sequence data are lacking. Here, we used 3,078 metagenomes to analyze the distribution of PHA depolymerases in microbial communities from diverse aquatic, terrestrial and waste management systems. We significantly expand the recognized diversity of this protein family by screening 1,914 Gb of sequence data and identifying 13,869 putative PHA depolymerases in 1,295 metagenomes. Our results indicate that PHA depolymerases are unevenly distributed across environments. We predicted the highest frequency of PHA depolymerases in wastewater systems and the lowest in marine and thermal springs. In tandem, we screened 5,290 metagenome-assembled genomes to describe the phylogenetic distribution of PHA depolymerases, which is substantially broader compared to current cultured representatives. The Proteobacteria and Bacteroidota are key lineages encoding PHA depolymerases, but PHA depolymerases were predicted from members of the Bdellovibrionota, Methylomirabilota, Actinobacteriota, Firmicutes, Spirochaetota, Desulfobacterota, Myxococcota and Planctomycetota. Originality/Significance StatementBiodegradable plastics like polyhydroxyalkanoates (PHAs) are a hot topic, following ubiquitous environmental plastic contamination, government bans on single-use plastics, and a growing need for sustainable alternatives to petroleum-based plastics. Understanding the microbial conversion of PHAs in the environment and finding biomolecular tools that can act on PHAs is increasingly important as PHAs grow in popularity. In this study, we screened thousands of metagenomes and metagenome-assembled genomes (MAGs) to substantially increase the recognized diversity of PHA depolymerases, the key enzymes mediating PHA biodegradation. We use datasets from seven continents to provide a global summary of the distribution of PHA depolymerase genes in natural environments and waste-management systems. In tandem, we increase the number of described phylum-level lineages with PHA biodegradation potential. This work contributes a new understanding of the phylogenetic and environmental distribution of PHA depolymerases.