Unveiling deep-sea biodegradation of microbially produced lactate-based polyester (LAHB) via plastisphere metagenomics and metatranscriptomics

Abstract

A representative bio-based polyester, polylactide (PLA), is widely used but known to resist marine degradation. Recently, a lactate-based polyester, poly(D-lactide-co-3-hydroxybutyrate) (LAHB), has been biosynthesized by recombinant Escherichia coli, showing biodegradability in soil, river water, and shallow seawater. In this study, deep-sea biodegradability of two LAHB films (6 % and 13 % LA-contained) at water depth of 855 m and the biodegradation scheme were investigated using genome-centric metatranscriptomic analyses of plastisphere microbiomes. Even at the deep-sea floor, both LHABs were degraded with time, and dense biofilms were established on the film surfaces. From the plastisphere metagenomic analyses, four Gammaproteobacterial genera were correlated with LAHB, indicating material-specific microbial enrichment within the LAHB biofilms. A total of 37 metagenome-assembled genomes (MAGs) were identified from the LAHB plastispheres, while three Gammaproteobacterial MAGs possessed numerous amounts of secretion-type PHB depolymerases. In situ gene expression profiles revealed that a wide variety of the PHB depolymerases were highly transcribed, suggesting that they played key roles in LAHB biodegradation. Notably, a LAHB-preferable microbe affiliated with genus UBA7957 showed strong transcriptional activity of a gene cluster including dimer hydrolase, a putative transporter, and propionyl CoA-transferase, likely involved in the oceanic LAHB biodegradation. These findings outlined a biodegradation scheme of LAHB at the deep-sea floor, highlighting the involvement of specific microbes and enzymes. This study revealed the possibility that LAHB can be biodegraded and mineralized under deep-sea environments through cooperative microbial metabolism within the plastisphere, expanding the potential for sustainable biodegradable plastics.