Cross-Hemisphere Study Reveals Geographically Ubiquitous, Plastic-Specific Bacteria Emerging from the Rare and Unexplored Biosphere

Abstract

While it is now appreciated that the millions of tons of plastic pollution travelling through marine systems carry complex communities of microorganisms, it is still unknown to what extent these biofilm communities are specific to the plastic or selected by the surrounding ecosystem. To address this, we characterized and compared the microbial communities of microplastic particles, nonplastic (natural and wax) particles, and the surrounding waters from three marine ecosystems (the Baltic, Sargasso and Mediterranean seas) using high-throughput 16S rRNA gene sequencing. We found that biofilm communities on microplastic and nonplastic particles were highly similar to one another across this broad geographical range. The similar temperature and salinity profiles of the Sargasso and Mediterranean seas, compared to the Baltic Sea, were reflected in the biofilm communities. We identified plastic-specific operational taxonomic units (OTUs) that were not detected on nonplastic particles or in the surrounding waters. Twenty-six of the plastic-specific OTUs were geographically ubiquitous across all sampled locations. These geographically ubiquitous plastic-specific OTUs were mostly low-abundance members of their biofilm communities and often represented uncultured members of marine ecosystems. These results demonstrate the potential for plastics to be a reservoir of rare and understudied microbes, thus warranting further investigations into the dynamics and role of these microbes in marine ecosystems. IMPORTANCE This study represents one of the largest comparisons of biofilms from environmentally sampled plastic and nonplastic particles from aquatic environments. By including particles sampled through three separate campaigns in the Baltic, Sargasso, and Mediterranean seas, we were able to make cross-geographical comparisons and discovered common taxonomical signatures that define the plastic biofilm. For the first time, we identified plastic-specific bacteria that reoccur across marine regions. Our data reveal that plastics have selective properties that repeatedly enrich for similar bacteria regardless of location, potentially shifting aquatic microbial communities in areas with high levels of plastic pollution. Furthermore, we show that bacterial communities on plastic do not appear to be strongly influenced by polymer type, suggesting that other properties, such as the absorption and/or leaching of chemicals from the surface, are likely to be more important in the selection and enrichment of specific microorganisms.

Keywords: Rhodobacteraceae; bacterial communities; biofilms; marine microbiology; microbiome; microplastics.

FIG 1

Map of sampling locations. Red dots indicate sampling stations.

FIG 2

Principal-coordinate analysis (PCoA) of bacterial communities from plastic particles, natural particles, wax particles, particle-associated (>3 μm) water fractions, and free-living (3 μm to 0.22 μm) water fractions. The Bray-Curtis distance metric, which takes into account both abundances and presence/absences of individual OTUs, was used to measure the dissimilarity of each sample. Each symbol refers to a bacterial community. The individual communities are colored based on sample type and have different shapes based on location. More similar communities are closer together in the ordination plot. Results of PERMANOVA and homogeneity of dispersion analysis are found in Table S1.

FIG 3

PCoA of bacterial communities on plastic, natural, and wax particles, colored by specific particle type. Bray-Curtis distance metrics were used to measure the dissimilarity of each sample. Each symbol refers to an individual bacterial community. The individual communities are colored based on the type of plastic type and have different shapes based on location. More similar communities are closer together in the ordination plot. Results of PERMANOVA and homogeneity of dispersion analysis are found in Table S1. ABS, acrylonitrile butadiene styrene; HDPE, high-density polyethylene; PP, polypropylene; PAAM, polyacrylamide; PE, polyethylene; PET, polyethylene terephthalate; PS, polystyrene; PVC, polyvinyl chloride; PU, polyurethane; TEF, thermoplastic elastomer fiber.

FIG 4

Discovery of plastic-specific OTUs found across all three locations. (a) A total of 2,280 OTUs were present in plastic biofilms but absent from all other sample types in this study. (b) Of the plastic-specific OTUs, 26 were found on samples from all three locations. (c) Relative abundances of the 26 plastic-specific OTUs found across all locations. Each dot refers to a single plastic biofilm community.

FIG 5

Plastic-specific bacteria and their nearest neighbors. Phylogenetic tree of the 26 plastic-specific OTUs found across all three sampling locations and their nearest neighbors. The plastic biofilms that contain each OTU are depicted by the circles and are colored by location; turquoise indicates that the samples were taken from the Baltic Sea, light green indicates the Mediterranean, and maroon indicates the Sargasso. The size of the dot corresponds to the abundance of that OTU in the sample. Information on the nearest neighbors was obtained from NCBI, and patterns of isolation sources are depicted by highlighting. Nearest neighbors collected from oil spills are highlighted in purple, and those associated with various eukaryotes are in yellow. Neighbor-joining bootstrap tree based on 1,000 iterations, displaying confidence values of >50%. The tree was built in ARB. The bar represents 10 nucleotide substitutions per 100 nucleotides.