Unique plastisphere viromes with habitat-dependent potential for modulating global methane cycle

Abstract

Plastispheres, novel niches in the Anthropocene, harbor microbial communities with unique functional signatures. As the most abundant biological entity on Earth, viruses are key regulators of microbial community composition and metabolism. However, little is known about viral communities and their functions in the plastisphere. Here, we investigate the composition and functional profile of plastisphere viral communities through microcosm experiments combined with global plastisphere metagenomics data. We find that the plastisphere recruits a distinct viral community with 86.9% novel viral operational taxonomic units compared to control substrates. The plastisphere viral community modulates host methane metabolism through auxiliary metabolic genes and distinctive interactions with hosts. These auxiliary metabolic genes for methane cycling are prevalent in global plastisphere viral communities. Notably, the plastisphere microbiome adopts the life history strategy of copiotrophs in the nutrient-poor water environment, making the water plastisphere a potential hot spot for methane emission compared to the soil plastisphere. Our phage transplantation experiments reveal that lysogenic viruses significantly contribute to enhancing the methanogenic capacity of microorganisms and promoting methane emission of the water plastisphere. Overall, we decipher the role of viruses in the plastisphere and reinforce the necessity of incorporating viral contributions when assessing the effects of plastisphere communities on global biogeochemical cycles.