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Viral lysing can alleviate microbial nutrient limitations and accumulate recalcitrant dissolved organic matter components in soil

The ISME Journal volume 17, pages 1247–1256 (2023)Cite this article

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Abstract

Viruses are critical for regulating microbial communities and biogeochemical processes affecting carbon/nutrient cycling. However, the role of soil phages in controlling microbial physiological traits and intrinsic dissolved organic matter (DOM) properties remains largely unknown. Herein, microcosm experiments with different soil phage concentrates (including no-added phages, inactive phages, and three dilutions of active phages) at two temperatures (15 °C and 25 °C) were conducted to disclose the nutrient and DOM dynamics associated with viral lysing. Results demonstrated three different phases of viral impacts on CO2 emission at both temperatures, and phages played a role in maintaining Q10 within bounds. At both temperatures, microbial nutrient limitations (especially P limitation) were alleviated by viral lysing as determined by extracellular enzyme activity (decreased Vangle with active phages). Additionally, the re-utilization of lysate-derived DOM by surviving microbes stimulated an increase of microbial metabolic efficiency and recalcitrant DOM components (e.g., SUV254, SUV260 and HIX). This research provides direct experimental evidence that the “viral shuttle” exists in soils, whereby soil phages increase recalcitrant DOM components. Our findings advance the understanding of viral controls on soil biogeochemical processes, and provide a new perspective for assessing whether soil phages provide a net “carbon sink” vs. “carbon source” in soils.

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Fig. 1: Dynamics of CO2 emission rate (mean ± std dev) with added viruses incubated over 98 days.
Fig. 2: Carbon use efficiency (CUE) (mean ± std dev).
Fig. 3: Microbial resource acquisition strategies.
Fig. 4: Changes of recalcitrant DOM components (mean ± std dev) after incubation.
Fig. 5: Mean predictor importance (percent increased mean square error, MSE) for microbial metabolic indexes, besed on Random Forest analysis.
Fig. 6: Correlation networks between measured variables (e.g., Vangle, SUV254, SUV260 and HIX) and associated bacterial taxa.

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Data availability

The original sequence data were deposited into the National Center for Biotechnology Information Sequence Read Archive database under project ID PRJNA974558. Experimental data have been included as a supplement to this publication.

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (41721001, 41991334), the Science and Technology Program of Zhejiang Province (2022C02046), the 111 Project (B17039), and China Agriculture Research System (CARS-01).

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Authors and Affiliations

  1. Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, China

    Di Tong, Youjing Wang, Haodan Yu, Haojie Shen & Jianming Xu

  2. Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou, 310058, China

    Di Tong, Youjing Wang, Haodan Yu, Haojie Shen & Jianming Xu

  3. Department of Land, Air and Water Resources, University of California, Davis, CA, USA

    Randy A. Dahlgren

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Contributions

Design of experiment: JX; soil sampling and microcosm incubation: DT, YW and HY; measurement of soil properties: DT and HS; statistical analysis: DT; visualization: DT; writing—original draft: DT and JX; writing—review and editing: JX, RA. Dahlgren and DT.

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Correspondence to Jianming Xu.

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Tong, D., Wang, Y., Yu, H. et al. Viral lysing can alleviate microbial nutrient limitations and accumulate recalcitrant dissolved organic matter components in soil. ISME J 17, 1247–1256 (2023). https://doi.org/10.1038/s41396-023-01438-5

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  • DOI: https://doi.org/10.1038/s41396-023-01438-5

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