Soil viral–host interactions regulate microplastic-dependent carbon storage

Microplastic is globally regarded as an important factor impacting biogeochemical cycles, yet our understanding of such influences is limited by the uncertainties of intricate microbial processes. By multiomics analysis, coupled with soil chemodiversity characterization and microbial carbon use efficiency (CUE), we investigated how microbial responses to microplastics impacted soil carbon cycling in a long-term field experiment. We showed that biodegradable microplastics promoted soil organic carbon accrual by an average of 2.47%, while nondegradable microplastics inhibited it by 17.4%, as a consequence of the virus-bacteria coadaptations to the microplastics disturbance. In the relevant functional pathways, nondegradable microplastics significantly (<i>P</i> < 0.05) enhanced the abundance and transcriptional activity related to complex carbohydrate metabolism, whereas biodegradable microplastics significantly (<i>P</i> < 0.05) promoted functions involved in amino acid metabolism and glycolysis. Accordingly, viral lysis enhanced in nondegradable microplastics treatments to introduce more complex organic compounds to soil dissolved organic matters, thus benefiting the oligotrophs with high carbon metabolic capabilities in exploitation competition. In contrast, biodegradable microplastics enriched viral auxiliary metabolic genes of carbon metabolism through "piggyback-the-winner" strategy, conferring to dominant copiotrophs, enhanced substrate utilization capabilities. These virus-host interactions were also demonstrated in the corresponding soil plastisphere, which would alter microbial resource allocation and metabolism via CUE, affecting carbon storage consequently. Overall, our results underscore the importance of viral-host interactions in understanding the microplastics-dependent carbon storage in the soil ecosystem.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-10-28
DOI
https://doi.org/10.1073/pnas.2413245121
Citations
70
Primary Topic
Bacteriophages and microbial interactions
Type
article
Field-Weighted Citation Impact
32.12

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article

Soil viral–host interactions regulate microplastic-dependent carbon storage

Yanjie Liu, Lijuan Ma, Yanmei Fu, Mingming Sun et al.
70 citations
Proceedings of the National Academy of Sciences
Bacteriophages and microbial interactions
32.12
article

Soil viral–host interactions regulate microplastic-dependent carbon storage

Yanjie Liu, Lijuan Ma, Yanmei Fu, Mingming Sun, Ke‐Qing Xiao, Matthias C. Rillig, Dong Zhu, Da Lin, Lu Wang, Yong‐Guan Zhu, Mao Ye, Yan Huo
article en
70 citations

Abstract

Microplastic is globally regarded as an important factor impacting biogeochemical cycles, yet our understanding of such influences is limited by the uncertainties of intricate microbial processes. By multiomics analysis, coupled with soil chemodiversity characterization and microbial carbon use efficiency (CUE), we investigated how microbial responses to microplastics impacted soil carbon cycling in a long-term field experiment. We showed that biodegradable microplastics promoted soil organic carbon accrual by an average of 2.47%, while nondegradable microplastics inhibited it by 17.4%, as a consequence of the virus-bacteria coadaptations to the microplastics disturbance. In the relevant functional pathways, nondegradable microplastics significantly (<i>P</i> < 0.05) enhanced the abundance and transcriptional activity related to complex carbohydrate metabolism, whereas biodegradable microplastics significantly (<i>P</i> < 0.05) promoted functions involved in amino acid metabolism and glycolysis. Accordingly, viral lysis enhanced in nondegradable microplastics treatments to introduce more complex organic compounds to soil dissolved organic matters, thus benefiting the oligotrophs with high carbon metabolic capabilities in exploitation competition. In contrast, biodegradable microplastics enriched viral auxiliary metabolic genes of carbon metabolism through "piggyback-the-winner" strategy, conferring to dominant copiotrophs, enhanced substrate utilization capabilities. These virus-host interactions were also demonstrated in the corresponding soil plastisphere, which would alter microbial resource allocation and metabolism via CUE, affecting carbon storage consequently. Overall, our results underscore the importance of viral-host interactions in understanding the microplastics-dependent carbon storage in the soil ecosystem.

Proceedings of the National Academy of SciencesVol. 121(45)
Nanjing Agricultural University (CN), Chinese Academy of Sciences (CN), Northeast Institute of Geography and Agroecology (CN), Berlin Brandenburg Institute of Advanced Biodiversity Research (DE), Institute of Urban Environment (CN), Research Center for Eco-Environmental Sciences (CN), University of Chinese Academy of Sciences (CN), Institute of Soil Science (CN), Hebei University (CN), Freie Universität Berlin (DE)
Department of Science and Technology, Ministry of Science and Technology, India, National Natural Science Foundation of China, Chinese Academy of Sciences, Youth Innovation Promotion Association of the Chinese Academy of Sciences, Youth Innovation Promotion Association
Responsible consumption and production
Openalex Percentile: Top 0%
Bacteriophages and microbial interactions
32.12
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