Plastics in the environment represent new substrates for microbial colonization, and recent methodological advances allow for in-depth characterization of plastic-associated microbial communities (PAMCs). Over the past several decades, discovery of plastic degrading enzymes (PDEs) and plastic degrading microorganisms (PDMs) has been driven by efforts to understand microbially-mediated plastic degradation in the environment and to discover biocatalysts for plastic processing. In this review, we discuss the evolution of methodology in plastic microbiology and highlight major advancements in the field stemming from computational microbiology. Initial research relied largely on culture-based approaches like clear-zone assays to screen for PDMs and microscopy to characterize PAMCs. New computational tools and sequencing technologies are accelerating discoveries in the field through culture-independent and multi-omic approaches, rapidly generating targets for protein engineering and improving the potential for plastic-waste management.

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 biobased 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 3078 metagenomes to analyse 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 1914 Gb of sequence data and identifying 13 869 putative PHA depolymerases in 1295 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 5290 metagenome-assembled genomes to describe the phylogenetic distribution of PHA depolymerases, which is substantially broader compared with current cultured representatives. The Proteobacteria and Bacteroidota are key lineages encoding PHA depolymerases, but PHA depolymerases were predicted from members of the Bdellovibrionota,

Polyhydroxyalkanoates (PHAs) are a family of microbially-made polyesters that have been commercialized as biodegradable plastics. PHA production rates are predicted to increase rapidly as global concerns around environmental plastic contamination and limited fossil fuel resources have increased the importance of bio-based plastic alternatives. PHAs are meant to quickly degrade in the environment, but this degradation is reliant on microbially-secreted PHA depolymerases, whose taxonomic and environmental distribution have not been well-defined. As a result, the impact of increased PHA production and disposal on global environments is unknown. Here we used 3,842 metagenomes to analyze the distribution of PHA depolymerase genes in microbial communities from diverse aquatic, terrestrial and waste management systems. Our results indicate that extracellular PHA depolymerases are globally widespread but unevenly distributed, with certain environments showing little to no evidence for this activity. In tandem, we screened 5,290 metagenome-assembled genomes to describe the phylogenetic distribution of this trait, which is substantially broader compared to current cultured representatives. We identified members of the Proteobacteria and Bacteroidetes as key lineages with PHA biodegradation potential and predict this activity in members of the Actinobacteria, the Candidate phylum Rokubacteria, Firmicutes, Planctomycetes and Spirochaetes.ImportanceEnvironmental concerns alongside legislation banning single-use petroleum-based plastics are expected to promote the production of bio-based plastics, including PHAs. PHAs represent a novel and emerging waste stream. If PHA disposal follows the precedent set by conventional plastics, a significant portion will be littered into the environment, or improperly discarded into landfills instead of composting facilities. Traditionally, the identification of bioplastic degrading enzymes and organisms has relied on culture-dependent assays. As a result, the PHA degradation capabilities of the “unculturable” fraction of microorganisms remain largely unexplored. Here, we leverage large amounts of environmental sequence data to assess which environments harbor PHA-degrading organisms and to determine the taxonomic affiliations of bioplastic degraders. Our analyses inform our understanding of the biodegradation potential in the environment, with implications for the impact of bioplastic pollution. We identify enzymes and organisms that may be suitable for future bioremediation, chemical processing or biotechnological applications.