Rapid Evolution of Plastic-degrading Enzymes Prevalent in the Global Ocean

Abstract

Estimates of marine plastic stocks, a major threat to marine life (1), are far lower than expected from exponentially-increasing litter inputs, suggesting important loss factors (2, 3). These may involve microbial degradation, as the plastic-degrading polyethylene terephthalate enzyme (PETase) has been reported in marine microbial communities (4). An assessment of 416 metagenomes of planktonic communities across the global ocean identifies 68 oceanic PETase variants (oPETase) that evolved from ancestral enzymes degrading polycyclic aromatic hydrocarbons. Twenty oPETases show predicted efficiencies comparable to those of laboratory-optimized PETases, suggesting strong selective pressures directing the evolution of these enzymes. We found oPETases in 90.1% of samples across all oceans and depths, particularly abundant at 1,000 m depth, with a strong dominance of Pseudomonadales containing putative highly-efficient oPETase variants in the dark ocean. Enzymatic degradation may be removing plastic from the marine environment while providing a carbon source for bathypelagic microbial communities.

Plastic-degrading potential across the global microbiome correlates with recent pollution trends

“…Comparison of the ocean and soil fractions shows that the uncovered enzymatic potential likely reflects the major differences related to the composition of these two environments. Further analysis of metagenome-assembled genomes in the ocean reveals a significant enrichment of plastic-degrading enzymes within members of the Alpha-and Gamma-proteobacteria classes, and supports the notion that enzyme abundance increases with depth as a response to plastic pollution and not merely taxonomic composition [47][48][49] . By relating the identified enzymes to the respective habitats and measured environmental variables within the soil and ocean environments, we further show that the abundance of the uncovered enzymes significantly correlates with both marine and country-specific plastic pollution measurements 50-55 , suggesting that the earth's microbiome might already be adapting to current global plastic pollution trends.…”

“…To minimize the number of false positive hits, we used the gut microbiome 46 as a negative control (Figure 1c), that is, we assumed that the gut microbiome is not evolved to degrade plastics and thus enzyme hits that are similar to the ones found in the human gut would indicate false positives. Nearly 60% of identified plastic-degrading enzymes did not map to any known enzyme classes (Figure 1f), suggesting that novel plastic-degrading functional content was uncovered, which is not surprising considering the vast amounts of novel functions being uncovered in recent large-scale metagenomic studies [33][34][35]49 .…”

“…Firstly, we find that taxonomic and functional richness is likely not the only driver of the observed depth stratification of enzyme hits (Figure 2c). The organisms found to carry the largest amount of plastic-degrading enzymes (Figure 2d) do not completely reflect initial taxonomic estimates in the ocean 35 , indicating that the plastic-degrading potential also reflects the recently uncovered trends of an increasing amount of plastic pollution below the surface (<200m) 48 with considerable microplastic pollution in the mesopelagic zone 47 , which are potentially stronger drivers of the observed depth stratification 49 . Secondly, certain habitats containing the highest amounts of observed enzyme hits, such as the Mediterranean Sea and South Pacific Ocean (Figure 2a), are known to be highly polluted areas 52,67 .…”

“…Plastics have been increasingly mass produced ever since the economic and social explosion after the 2 nd world war with the first signs of global plastic pollution concern arising over half a century ago 68,69 , giving ample evolutionary time for microbial functional adaptation to these compounds 49,76,77 . Such adaptation was recently uncovered with PET-degrading enzymes across ocean metagenomes of planktonic communities 49 , where multiple fully-functional enzyme variants were found to be evolved from ancestral enzymes degrading polycyclic aromatic hydrocarbons, suggesting that the current PET exposure already provides sufficiently strong selective pressures to direct the evolution and repurposing of such enzymes. Similarly, enzymes degrading other plastic types have been shown to be widely occurring with numerous homologs in diverse organisms and likely arising from well conserved general enzyme classes 78,79 .…”

“…within Alpha-and Gamma-proteobacteria, which can be expected since this is the most Zrimec et al 2020 9 abundant and diverse phylum in the dataset (Figure 2d, Table S4). Nevertheless, the results suggested that the observed plastic-degrading enzyme abundance (Figure 2d) might not be a reflection of merely taxonomic and functional richness, but also of recently uncovered large amounts of plastic pollution below the ocean surface [47][48][49] .…”