Metagenomic and metatranscriptomic analyses reveal uncharted microbial constituents responsible for polyhydroxybutyrate biodegradation in coastal waters

Polyhydroxybutyrate (PHB) has attracted attention as a representative polymer for biodegradable plastics produced by microorganisms. Since information regarding the fate of PHB released into the environment is limited, it is necessary to identify them based on metagenomic information. We estimated the PHB biodegradability in coastal water samples collected from 15 near shore sites around Japan using oxygen consumption as an indicator in laboratory-scale incubation experiments and conducted 16S rRNA gene-based microbial community profiling. The PHB-biodegradation-rate was significantly positively correlated with the diversity indices of the microbial community in seawater prior to incubation, indicating that seawater with higher diversity is more advantageous for biodegradation. We identified 41 operational taxonomic units exhibiting a significant positive correlation between their abundance and PHB-degradation-rates; these included several microorganisms with hitherto unreported PHB-degrading ability. Next, we analyzed gene expression patterns over incubation time using seawater samples employing metagenomic and metatranscriptomic approaches. Fifty-seven putative extracellular PHB/PHA depolymerase genes were found in 38 metagenomic bins and their expression changed with increasing biodegradation rates, indicating that PHB released into the marine environment is subject to degradation by phylogenetically diverse PHB-depolymerase-producing bacteria. These findings should contribute to expanding the knowledge on degradation of biodegradable plastics by complex marine microbial ecosystems.