Phylogenetic Distribution of Plastic-Degrading Microorganisms

Abstract

The number of plastic-degrading microorganisms reported is rapidly increasing, making it possible to explore the conservation and distribution of presumed plastic-degrading traits across the diverse microbial tree of life. Putative degraders of conventional high-molecular-weight polymers, including polyamide, polystyrene, polyvinylchloride, and polypropylene, are spread widely across bacterial and fungal branches of the tree of life, although evidence for plastic degradation by a majority of these taxa appears limited. In contrast, we found strong degradation evidence for the synthetic polymer polylactic acid (PLA), and the microbial species related to its degradation are phylogenetically conserved among the bacterial family Pseudonocardiaceae We collated data on genes and enzymes related to the degradation of all types of plastic to identify 16,170 putative plastic degradation orthologs by mining publicly available microbial genomes. The plastic with the largest number of putative orthologs, 10,969, was the natural polymer polyhydroxybutyrate (PHB), followed by the synthetic polymers polyethylene terephthalate (PET) and polycaprolactone (PCL), with 8,233 and 6,809 orthologs, respectively. These orthologous genes were discovered in the genomes of 6,000 microbial species, and most of them are as yet not identified as plastic degraders. Furthermore, all these species belong to 12 different microbial phyla, of which just 7 phyla have reported degraders to date. We have centralized information on reported plastic-degrading microorganisms within an interactive and updatable phylogenetic tree and database to confirm the global and phylogenetic diversity of putative plastic-degrading taxa and provide new insights into the evolution of microbial plastic-degrading capabilities and avenues for future discovery.IMPORTANCE We have collated the most complete database of microorganisms identified as being capable of degrading plastics to date. These data allow us to explore the phylogenetic distribution of these organisms and their enzymes, showing that traits for plastic degradation are predominantly not phylogenetically conserved. We found 16,170 putative plastic degradation orthologs in the genomes of 12 different phyla, which suggests a vast potential for the exploration of these traits in other taxa. Besides making the database available to the scientific community, we also created an interactive phylogenetic tree that can display all of the collated information, facilitating visualization and exploration of the data. Both the database and the tree are regularly updated to keep up with new scientific reports. We expect that our work will contribute to the field by increasing the understanding of the genetic diversity and evolution of microbial plastic-degrading traits.

Keywords: biodegradation; phylogenetic distribution; plastic.

FIG 1

Phylogenetic tree showing all microorganisms identified as having potential plastic-degrading capabilities. The phylogenetic relationship among species was downloaded from the NCBI taxonomy database. Leaves are colored according to their corresponding phyla. Data points plotted outside the tree represent the ability of each microorganism to degrade each of the plastics shown in the key. The key order from top to bottom is the same as the order of rings external to the tree, from the inside to the outside. Bacteria belonging to the family Pseudonocardiaceae and the order Bacillales are identified by thicker branches on the tree. The phylogenetic relationship among the reported degraders was extracted from the NCBI taxonomic database classification system. An interactive version of the tree with all plastic types is available at http://itol.embl.de/shared/gambarini with the code P1. All trees used in this publication are each accessible via this website, from P1 to P5; chronologically updated trees are also available and are termed U1 to U3.

FIG 2

Relative abundances of all taxa reported to degrade plastics at the levels of domain (A), phylum (B), and class (C).

FIG 3

Phylogenetic tree showing the abundances of genes similar to those encoding Saccharomonospora viridis cutinase and Paenibacillus amylolyticus and uncultured bacterium PLA depolymerases in all microorganisms with reported plastic-degrading capabilities. Leaves are colored according to phylum. The solid black squares plotted directly around the outside of the tree indicate the availability of genomes in the NCBI genome database. Green bars represent the number of genes found within a genome that are similar to the gene encoding Paenibacillus amylolyticus PLA depolymerase, blue bars represent those with genes encoding products similar to Saccharomonospora viridis cutinase that has activity against PLA, and yellow bars represent genes similar to a PLA depolymerase from an uncultured bacterium. The key order from top to bottom is the same as the order of rings external to the tree, from the inside to the outside. An interactive version of the tree, with all putative genes related to plastic degradation found by this study, is available at http://itol.embl.de/shared/gambarini with the code P2.