The Uniqueness Of The Plastisphere Microbiome And Its Ecological Risks

Due to its high malleability,low cost,waterproof,insulation,as well as high resistance to corrosion and impact,plastic has been widely used in all aspects of human life.Global annual production of plastic products has climbed from 1.5 million tons in 1950 to nearly 400 million tons in 2021 and continues growing.Only a small proportion of plastic waste can be recycled,while the majority(～80%)of it ends up in landfills or the natural environment.Large emissions and the poor degradability of plastic waste have resulted in a huge and growing amount of plastic waste in the environment.Plastics in the environment gradually break down into smaller plastics through physical,chemical,and biological processes,eventually forming microplastics(plastic particles<5 mm).Due to their smaller particle size,microplastics are easier to enter the food chain and are more widely distributed in the environment,which could cause more serious ecological consequences.Therefore,it is urgent to clarify the ecological impacts of microplastics with a view to managing their ecological risks.(Micro)plastics in the environment provide a new ecological niche for microorganisms to colonize,and this new human-made ecosystem is referred to as "the plastisphere".The size of individual plastic being able to enter the food chain means that the plastisphere can carry microorganisms into organisms causing combined effects while large emissions,the poor degradability of plastic waste in the environment mean that the plastisphere is a new habitat with a vast,expanding area and hosts a significant microbial biomass.Microorganisms shape the processes and functions of ecosystems at all times,and regulates the health of plants,animals and all humans.Therefore,elucidating the impact of(micro)plastic pollution on ecosystem functioning and health through the formation of the plastisphere microbiome is essential for a comprehensive assessment of(micro)plastic pollution risks and the development of informed strategies thus achieving a sustainable future.Based on literature survey,metadata analysis,field sampling,genebank big-data analysis together with techniques including amplicon sequencing and metagenomic sequencing,this study deciphering the distribution characteristics of environmental microplastics,the plastisphere microbial ecology,the antibiotic resistance risk from the plastisphere,and the threats of the plastisphere to ecosystem functioning and "One Health".The main contents and findings are as follows:(1)We proposed a new concept of "icroplastic community" and applied the thinking in community ecology to characterize the complex and diverse microplastics in the environment.By analyzing microplastic data of 709 sampling points from five major microplastic environmental reservoirs(namely,freshwater,seawater,freshwater sediment,sea sediment.and soil),we found that the abundance of microplastics in freshwater(mean:6829 items·m-3)was significantly higher than that in seawater(mean:1320 items·m-3),and the abundance of microplastics in soil(mean:1.6e5 items·kg-1)was significantly higher than that in freshwater sediment(mean:436 items·kg-1)as well as that in sea sediment(mean:487 items·kg-1).Compared with the other four ecosystems,the particle size of microplastics in seawater ecosystem was significantly larger.Fiber and fragment were the main shapes of microplastics and transparent was the dominant microplastic color in each ecosystem.Polyethylene(PE)and polypropylene(PP)were the dominant microplastic polymers in each ecosystem.The composition of microplastics varied significantly among different ecosystems but interacted with each other,reflecting the "microplastic cycle"and the long-distance.cross-ecosystem transport property of microplastics in the environment.Based on the diversity of microplastic shape,color,and polymer types,we established a microplastic diversity integrated index(MDII).Then we verified the positive correlation between this index and the number of industrial pollution sources,indicating that this index could reflect the complexity of both the pollution conditions and potential sources of microplastics,and this index can be used in future studies for characterization and source analysis of environmental microplastics.(2)Through field sample collection,amplicon sequencing,and environmental parameter detection of plastic debris and its surrounding water samples from freshwater and seawater ecosystems.we analyzed the uniqueness of diversity.composition.assembly mechanisms,and taxonomic structure drivers of bacterial and fungal communities in the plastisphere and explored the mechanisms underlying the uniqueness.We found that,in both freshwater and seawater ecosystems,the bacterial diversity was significantly higher while the fungal diversity was significantly lower in the plastisphere than in the bulk environment.Significant difference existed in the community composition between the plastisphere and the bulk environment.The plastisphere selectively enriched its preferred microbial populations resulting in a reshaping of the microbial community structure in it.A large number of unique taxa in the plastisphere indicated that the plastisphere could carry and harbor microorganisms for long-distance transport,which might cause a microbial invasion risk.There were significant differences in microbial functional signatures between the plastisphere and the bulk environment,with differential functions including pathogenicity,compound degradation potential,and functions related to carbon,nitrogen,and sulfur cycling.The oxidation-reduction potential,salinity,the concentrations of nitrogen-related ions(NO3-,NO2-,and NH4+),and the concentration of dissolved organic carbon in the bulk environment drove the structural variation of the plastisphere microbiome.But environmental physicochemical properties explain less of the structural variation in the plastisphere than that in the aquatic environment,reflecting the sheltering role of the plastisphere for microorganisms once more.Deterministic processes dominated the assembly of the plastisphere microbial community,and the role of deterministic processes in the plastisphere was significantly higher than that in the bulk environment,which could be attributed to the fact that the high heterogeneity of the plastisphere increased the environmental filtering and thus increased the relative importance of determinism,while the fragmentation of the plastisphere increased the dispersal limitation of microorganisms among different plastic debris and thus decreased the relative importance of stochasticity in the assembly.Therefore,it is clear that the unique physicochemical characteristics of plastic debris as a microbial habitat shape unique plastisphere microbial ecological patterns.(3)Based on the deep sequencing metagenomic data of 182 paired plastic debris and its bulk environment samples field collected across regions(Hong Kong coastal areas and Qingdao coastal areas)and seasons(wet and dry),we found that the total abundance,type richness and diversity of antibiotic resistance genes in the plastisphere were significantly higher than those in the bulk environment.The plastisphere selectively enriched its preferred antibiotic resistance genes,and among the top 8 major classes of antibiotic resistance genes,multidrug,macrolidelincosamide-streptogramin,bacitracin,beta-lactam,and vancomycin resistance were enriched in the plastisphere,while kasugamycin,tetracycline,and trimethoprim resistance genes did not differ significantly between the plastisphere and the bulk environment.There were 171 subtypes of resistance genes only occur in the plastisphere,indicating the long-distance transport of resistance genes carried by the plastisphere.The risks of human accessibility,mobility,human pathogenicity and clinical availability of antibiotic resistance genes in plastisphere were all significantly higher than those in the bulk environment,and the overall human health risk also showed significantly higher levels in the plastisphere.The resistome in the plastisphere was driven by geographic and seasonal factors,but it was less sensitive than the bulk environment,reflecting the sheltering role once more.The antibiotic pollution status and antibiotic resistance genes in the environment all showed positive correlations with the antibiotic resistance genes in the plastisphere.and the abundance,diversity and risk of antibiotic resistance genes in the plastisphere were significantly higher than the bulk environment.Therefore,it is clear that(micro)plastic pollution can exacerbate the risk of antibiotic resistance in the environment caused by the use and emission of antibiotics.(4)Based on field-collected samples and publicly available genetic databases,we established a global plastisphere dataset with samples covering freshwater,seawater,and terrestrial ecosystems.By mining the ecological patterns and functional characteristics of 1,013 samples of the plastisphere and the associated natural environment,we comprehensively revealed the potential ecological risks posed by the plastisphere.We found that the plastisphere assembled a distinct microbial community that had a clearly higher heterogeneity and a more deterministically-dominated assembly compared to natural habitats.New coexistence patterns-loose and fragile networks with mostly specialist linkages among microorganisms that were rarely seen in natural habitats-were yielded in the plastisphere.Plastisphere microbiomes generally had high potential to metabolize organic compounds,which could accelerate carbon turnover.Microorganisms involved in the nitrogen cycle were also altered in the plastisphere,especially in freshwater plastispheres,where a high abundance of denitrifiers could increase the release of nitrite(aquatic toxicant)and nitrous oxide(greenhouse gas).The recruiting of potential plant pathogens and animal parasites/symbionts in specific ecosystems,and the harboring of enriched and unique human pathogens means that the plastisphere could become an increasingly mobile reservoir of harmful microorganisms in the environment,posing critical challenges for "One Health."Overall,this study explored microplastic pollution characteristics in different ecosystems firstly and laid the foundation for the assessment of environmental microplastic contamination and for deciphering the formation mechanisms of the unique plastisphere microbiome.Based on this,this study revealed the microbial ecological patterns and their uniqueness in the new microbial habitat generated by environmental(micro)plastics—the plastisphere—at regional and global scales.The findings emphasize that the plastisphere might cause microbial invasion risks due to its ability of carrying microorganisms for long-distance.cross-ecosystem transport.poses critical challenges to "One Health" because it is a hotspot of antibiotic resistance genes and harmful microorganisms,and could disturb the functioning of natural ecosystems owing to its unique elemental metabolism signature.