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Viral metagenome reveals microbial hosts and the associated antibiotic resistome on microplastics

Abstract

Microplastics provide a unique niche for viruses, promoting viral interactions with hosts and accelerating the rapid ‘horizontal’ spread of antibiotic resistance genes (ARGs). Currently, however, there is a lack of knowledge concerning the main drivers for viral distribution on microplastics and on the resulting patterns of viral biogeographic distributions and the spread of the associated ARGs. Here we performed metagenomic and virus enrichment-based viromic sequencings on both polyethylene and polypropylene microplastics along a river. Experimental results show that Proteobacteria, Firmicutes, Actinobacteria and Cyanobacteria were the potential hosts of viruses on microplastics, but only approximately 4.1% of viral variations were associated with a bacterial community. Notably, two shared ARGs and six metal resistance genes were identified in both viral and their host bacterial genomes, indicating the occurrence of horizontal gene transfer between viruses and bacteria. Furthermore, microplastics introduce more distinctive elements to viral ecology, fostering viral diversification and virus–host linkage while refraining from an escalated level of horizontal gene transfer of ARGs in contrast to natural matrixes. Our study provides comprehensive profiles of viral communities, virus-related ARGs and their driving factors on microplastics, highlighting how these anthropogenic niches provide unique interfaces that comprise highly defined viral ecological features in the environment.

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Fig. 1: Diversity and composition of viral communities.
Fig. 2: Relative abundance of bacterial and viral-encoded resistance genes.
Fig. 3: MRG and taxonomic dynamics of bacterial and viral communities.
Fig. 4: Viral–host interaction structure.
Fig. 5: Comparisons of viral community composition, richness and evenness in natural particles and microplastics.

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Data availability

The raw sequencing reads of bacterial and viral communities have been deposited into the NCBI Sequence Read Archive (SRA) under the accession number PRJNA1104113 and PRJNA1104403 (https://www.ncbi.nlm.nih.gov/sra). The other data generated in this study are provided in the main text or Supplementary Information.

References

  1. Bank, M. S. & Hansson, S. V. The plastic cycle: a novel and holistic paradigm for the Anthropocene. Environ. Sci. Technol. 53, 7177–7179 (2019).

    Article  CAS  PubMed  Google Scholar 

  2. Kim, S. W., Waldman, W. R., Kim, T. & Rilling, M. C. Effects of different microplastics on nematodes in the soil environment: tracking the extractable additives using an ecotoxicological approach. Environ. Sci. Technol. 54, 13868–13878 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Yuan, W. et al. Tracing and trapping micro- and nanoplastics: untapped mitigation potential of aquatic plants? Water Res. 242, 120249 (2023).

    Article  CAS  PubMed  Google Scholar 

  4. Roman, L., Christoph, W., Alke, P. & Barbara, R. Emergence of nanoplastic in the environment and possible impact on human health. Environ. Sci. Technol. 53, 1748–1765 (2019).

    Article  Google Scholar 

  5. Frère, L. et al. Microplastic bacterial communities in the Bay of Brest: influence of polymer type and size. Environ. Pollut. 242, 614–625 (2018).

    Article  PubMed  Google Scholar 

  6. Zobell, C. E. & Anderson, D. Q. Observations on the multiplication of bacteria in different volumes of stored sea water and the influence of oxygen tension and solid surfaces. Biol. Bull. 71, 324–342 (1936).

    Article  Google Scholar 

  7. Zettler, E. R., Mincer, T. J. & Amaral-Zettler, L. A. Life in the ‘plastisphere’: microbial communities on plastic marine debris. Environ. Sci. Technol. 47, 7137–7146 (2013).

    Article  CAS  PubMed  Google Scholar 

  8. Zhu, D., Ma, J., Li, G., Rillig, M. C. & Zhu, Y.-G. Soil plastispheres as hotspots of antibiotic resistance genes and potential pathogens. ISME J. 16, 521–532 (2022).

    Article  CAS  PubMed  Google Scholar 

  9. Bank, M. S., Ok, Y. S. & Swarzenski, P. W. Microplastic’s role in antibiotic resistance. Science 369, 1315 (2020).

    Article  PubMed  Google Scholar 

  10. Lu, J., Yu, Z. G., Ngiam, L. & Guo, J. H. Microplastics as potential carriers of viruses could prolong virus survival and infectivity. Water Res. 225, 119115 (2022).

    Article  CAS  PubMed  Google Scholar 

  11. Ochirbat, E. et al. Heteroaggregation of virions and microplastics reduces the number of active bacteriophages in aqueous environments. J. Environ. Qual. 52, 665–677 (2023).

    Article  CAS  PubMed  Google Scholar 

  12. Moresco, V. et al. Binding, recovery, and infectiousness of enveloped and non-enveloped viruses associated with plastic pollution in surface water. Environ. Pollut. 308, 119594 (2022).

    Article  CAS  PubMed  Google Scholar 

  13. Li, R., Zhu, L., Cui, L. & Zhu, Y.-G. Viral diversity and potential environmental risk in microplastic at watershed scale: evidence from metagenomic analysis of plastisphere. Environ. Int. 161, 107146 (2022).

    Article  CAS  PubMed  Google Scholar 

  14. Chen, Y. et al. Prokaryotic viruses impact functional microorganisms in nutrient removal and carbon cycle in wastewater treatment plants. Nat. Commun. 12, 5398 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Pedro, B. et al. Dominance of phage particles carrying antibiotic resistance genes in the viromes of retail food sources. ISME J. 17, 195–203 (2022).

    Google Scholar 

  16. Debroas, D. & Siguret, C. Viruses as key reservoirs of antibiotic resistance genes in the environment. ISME J. 13, 2856–2867 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Christian, S. et al. Viromes outperform total metagenomes in revealing the spatiotemporal patterns of agricultural soil viral communities. ISME J. 15, 1956–1970 (2021).

    Article  Google Scholar 

  18. Amaral-Zettler, L. A., Zettler, E. R. & Mincer, T. J. Ecology of the plastisphere. Nat. Rev. Microbiol. 18, 139–151 (2020).

    Article  CAS  PubMed  Google Scholar 

  19. Ogonowski, M. et al. Evidence for selective bacterial community structuring on microplastics. Environ. Microbiol. 20, 2796–2808 (2018).

    Article  CAS  PubMed  Google Scholar 

  20. Cheng, J. et al. Relative influence of plastic debris size and shape, chemical composition and phytoplankton-bacteria interactions in driving seawater plastisphere abundance, diversity and activity. Front. Microbiol. 11, 610231 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Du, Y., Liu, X., Dong, X. & Yin, Z. A review on marine plastisphere: biodiversity, formation, and role in degradation. Comput. Struct. Biotechnol. J. 20, 975–988 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Li, H.-Q. et al. Soil pH has a stronger effect than arsenic content on shaping plastisphere bacterial communities in soil. Environ. Pollut. 287, 117339 (2021).

    Article  CAS  PubMed  Google Scholar 

  23. Chevallereau, A., Pons, B. J., van Houte, S. & Westra, E. R. Interactions between bacterial and phage communities in natural environments. Nat. Rev. Microbiol. 20, 49–62 (2022).

    Article  CAS  PubMed  Google Scholar 

  24. Liu, Z. et al. Viruses regulate microbial community assembly together with environmental factors in acid mine drainage. Appl. Environ. Microbiol. 89, e01973–01922 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Gao, S. et al. Patterns and ecological drivers of viral communities in acid mine drainage sediments across southern China. Nat. Commun. 13, 2389 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chen, M.-L. et al. Viral community and virus-associated antibiotic resistance genes in soils amended with organic fertilizers. Environ. Sci. Technol. 55, 13881–13890 (2021).

    Article  CAS  PubMed  Google Scholar 

  27. Wommack, K. E. et al. VIROME: a standard operating procedure for analysis of viral metagenome sequences. Stand. Genomic Sci. 6, 421–433 (2012).

    Article  CAS  Google Scholar 

  28. Finke, J. F., Hunt, B. P., Winter, C., Carmack, E. C. & Suttle, C. A. Nutrients and other environmental factors influence virus abundances across oxic and hypoxic marine environments. Viruses 9, 152 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Liang, X., Wang, Y., Zhang, Y., Zhuang, J. & Radosevich, M. Viral abundance, community structure and correlation with bacterial community in soils of different cover plants. Appl. Soil Ecol. 168, 104138 (2021).

    Article  Google Scholar 

  30. Han, L. et al. Genetic and functional diversity of ubiquitous DNA viruses in selected Chinese agricultural soils. Sci. Rep. 7, 45142 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Télesphore, S. Environmental bacteriophages: viruses of microbes in aquatic ecosystems. Front. Microbiol. 5, 355 (2014).

    Google Scholar 

  32. Lu, J. et al. Metagenomic analysis of viral community in the Yangtze River expands known eukaryotic and prokaryotic virus diversity in freshwater. Virol. Sin. 37, 60–69 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Marine, R. et al. Caught in the middle with multiple displacement amplification: the myth of pooling for avoiding multiple displacement amplification bias in a metagenome. Microbiome 2, 3 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Yang, Y., Li, T., Liu, P., Li, H. & Hu, F. The formation of specific bacterial communities contributes to the enrichment of antibiotic resistance genes in the soil plastisphere. J. Hazard. Mater. 436, 129247 (2022).

    Article  CAS  PubMed  Google Scholar 

  35. Wu, Z. Distinct adaptive strategies and microbial interactions of soil viruses under different metal(loid) contaminations. J. Hazard. Mater. 460, 132347 (2023).

    Article  CAS  PubMed  Google Scholar 

  36. Qi, R. et al. Heavy metal(loid)s shape the soil bacterial community and functional genes of desert grassland in a gold mining area in the semi-arid region. Environ. Res. 214, 113749 (2022).

    Article  CAS  PubMed  Google Scholar 

  37. Yao, Y. et al. Cross-regional scale pollution of freshwater biofilms unveiled by antibiotic resistance genes. Sci. Total Environ. 818, 151835 (2022).

    Article  CAS  PubMed  Google Scholar 

  38. Krupovic, M., Prangishvili, D., Hendrix, R. W. & Bamford, D. H. Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol. Mol. Biol. Rev. 75, 610–635 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Yuan, Q. et al. UV-aging of microplastics increases proximal ARG donor-recipient adsorption and leaching of chemicals that synergistically enhance antibiotic resistance propagation. J. Hazard. Mater. 427, 127895 (2022).

    Article  CAS  PubMed  Google Scholar 

  40. Liao, H. et al. Response of soil viral communities to land use changes. Nat. Commun. 13, 6027 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Li, Z. et al. Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity. ISME J. 15, 2366–2378 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Rillig, M. C., Kim, S. W. & Zhu, Y.-G. The soil plastisphere. Nat. Rev. Microbiol. 22, 64–74 (2023).

    Article  PubMed  Google Scholar 

  43. Adams, R. I., Bateman, A. C., Bik, H. M. & Meadow, J. F. Microbiota of the indoor environment: a meta-analysis. Microbiome 3, 49 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ter Horst, A. M., Fudyma, J. D., Sones, J. L. & Emerson, J. B. Dispersal, habitat filtering, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography. ISME J. 17, 2079–2089 (2023).

    Article  PubMed  Google Scholar 

  45. Xu, C., Lu, J., Shen, C., Wang, J. & Li, F. Deciphering the mechanisms shaping the plastisphere antibiotic resistome on riverine microplastics. Water Res. 225, 119192 (2022).

    Article  CAS  PubMed  Google Scholar 

  46. Castaño-Ortiz, J. M. et al. Fate of pharmaceuticals in the Ebro River Delta region: the combined evaluation of water, sediment, plastic litter, and biomonitoring. Sci. Total Environ. 906, 167467 (2024).

    Article  PubMed  Google Scholar 

  47. Andersson, D. I. et al. The biological cost of antibiotic resistance. Curr. Opin. Microbiol. 2, 489–493 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. Yang, K. et al. Temporal dynamics of antibiotic resistome in the plastisphere during microbial colonization. Environ. Sci. Technol. 54, 11322 (2020).

    Article  CAS  PubMed  Google Scholar 

  49. Li, R. et al. Impact of urbanization on antibiotic resistome in different microplastics: evidence from a large-scale whole river analysis. Environ. Sci. Technol. 55, 8760–8770 (2021).

    Article  CAS  PubMed  Google Scholar 

  50. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011).

    Article  Google Scholar 

  51. Li, D. et al. MEGAHIT v1. 0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 102, 3–11 (2016).

    Article  CAS  PubMed  Google Scholar 

  52. Noguchi, H., Taniguchi, T. & Itoh, T. MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res. 15, 387–396 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).

    Article  CAS  PubMed  Google Scholar 

  54. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Huson, D. H., Mitra, S., Ruscheweyh, H.-J., Weber, N. & Schuster, S. C. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552–1560 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Trubl, G. et al. Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils. PeerJ 7, e7265 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Adriaenssens, E. M. et al. Environmental drivers of viral community composition in Antarctic soils identified by viromics. Microbiome 51, 83 (2017).

    Article  Google Scholar 

  58. Bolger, A. M. et al. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Uritskiy, G. V., DiRuggiero, J. & Taylor, J. MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome 6, 158 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Edwards, R. A., McNair, K., Faust, K., Raes, J. & Dutilh, B. E. Computational approaches to predict bacteriophage–host relationships. FEMS Microbiol. Rev. 40, 258–272 (2016).

    Article  CAS  PubMed  Google Scholar 

  62. Pons, J. C. et al. VPF-Class: taxonomic assignment and host prediction of uncultivated viruses based on viral protein families. Bioinformatics 37, 1805–1813 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Laslett, D. & Canback, B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 32, 11–16 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinf. 10, 421 (2009).

    Article  Google Scholar 

  65. Seemann, T. et al. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Y.-G.Z.’s lab members were supported financially by the National Natural Science Foundation of China (42021005, 22193061, 21922608), Key Collaborative Research Program of the Alliance of International Science Organizations (ANSO-CR-KP-2020-03, ANSO-PA-2020-18) and Chinese Academy of Sciences (ZDBS-LY-DQC027).

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Authors

Contributions

R.L. designed the experiments and contributed to data analysis and the writing of the paper. X.-L.A. performed viral DNA extraction, sequencing and identification and the writing of the paper. Y.W. contributed to the creation of the final figures and the writing of the paper. Z.Y. contributed to the writing of the paper and discussion of results. J.-Q.S. contributed to the writing of the paper. J.C. contributed to the discussion of results. Y.-G.Z. conceived the idea of the study and contributed to the writing of the paper. All authors contributed to the review and editing of the paper.

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Correspondence to Yong-Guan Zhu.

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Nature Water thanks Bin Ma and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Information

Supplementary Tables 1 and 2 and Figs. 1–20.

Supplementary Data 1

Pathogenic bacteria.

Supplementary Data 2

Host–virus pairs.

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Li, R., An, XL., Wang, Y. et al. Viral metagenome reveals microbial hosts and the associated antibiotic resistome on microplastics. Nat Water 2, 553–565 (2024). https://doi.org/10.1038/s44221-024-00249-y

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