Bacteriophages (phages) influence biogeochemical cycling in soil ecosystems by mediating bacterial metabolism. However, the participation of phages in soil's overall ecological functions (multifunctionality) remains unclear. Hence, this study investigated the potential for phages and bacterial communities to shape the multifunctionality of compost-applied soils. The findings revealed that cow compost and vermicompost applications enhanced the soil's multifunctionality; consequently, the highest multifunctionality was observed in the soil with vermicompost application (p���<���0.05). The composition and diversity of bacteria and phages, as well as the abundance of functional genes of bacteria and phages related to carbon, nitrogen, phosphorus and sulphur metabolism, were dramatically altered following the application of both compost types. Moreover, the impact of phage diversity on soil multifunctionality is crucial for multi-threshold calculations. Structural equation modelling indicated that the effects of bacterial diversity on soil multifunctionality following compost application were paramount, with a path coefficient of 0.88 (p���<���0.01). The rise in phage diversity and the enrichment of functional genes indirectly led to a dramatic increase in the soil's ecological multifunctionality by affecting the host bacteria's metabolic processes. These results offer a novel avenue to improve soil's functions and environmental services by transforming the phage community composition and functions of soils.
Bin Jang, H., B. Bolduc, O. Zablocki, et al. 2019. ���Taxonomic Assignment of Uncultivated Prokaryotic Virus Genomes Is Enabled by Gene���Sharing Networks.��� Nature Biotechnology 37: 632���639.
Bolger, A. M., M. Lohse, and B. Usadel. 2014. ���Trimmomatic: A Flexible Trimmer for Illumina Sequence Data.��� Bioinformatics 30: 2114���2120.
Braga, L. P. P., A. Spor, W. Kot, et al. 2020. ���Impact of Phages on Soil Bacterial Communities and Nitrogen Availability Under Different Assembly Scenarios.��� Microbiome 8: 52.
Byrnes, J. E. K., L. Gamfeldt, F. Isbell, et al. 2014. ���Investigating the Relationship Between Biodiversity and Ecosystem Multifunctionality: Challenges and Solutions.��� Methods in Ecology and Evolution 5: 111���124.
Chao, H., J. L. Balcazar, Y. Wu, et al. 2023. ���Phages in Vermicomposts Enrich Functional Gene Content and Facilitate Pesticide Degradation in Soil.��� Environment International 179: 108175.
Chen, Y., Y. Zhang, X. Shi, et al. 2023. ���The Contribution of Earthworms to Carbon Mineralization During Vermicomposting of Maize Stover and Cow Dung.��� Bioresource Technology 368: 128283.
Chevallereau, A., B. J. Pons, S. Van Houte, and E. R. Westra. 2022. ���Interactions Between Bacterial and Phage Communities in Natural Environments.��� Nature Reviews Microbiology 20: 49���62.
Dai, Z., W. Su, H. Chen, et al. 2018. ���Long���Term Nitrogen Fertilization Decreases Bacterial Diversity and Favors the Growth of Actinobacteria and Proteobacteria in Agro���Ecosystems Across the Globe.��� Global Change Biology 24: 3452���3461.
Delgado���Baquerizo, M., F. T. Maestre, P. B. Reich, et al. 2016. ���Microbial Diversity Drives Multifunctionality in Terrestrial Ecosystems.��� Nature Communications 7: 10541.
Delgado���Baquerizo, M., P. B. Reich, C. Trivedi, et al. 2020. ���Multiple Elements of Soil Biodiversity Drive Ecosystem Functions Across Biomes.��� Nature Ecology & Evolution 4: 210���220.
Dion, M. B., F. Oechslin, and S. Moineau. 2020. ���Phage Diversity, Genomics and Phylogeny.��� Nature Reviews Microbiology 18: 125���138.
Dominguez���Huerta, G., A. A. Zayed, J. M. Wainaina, et al. 2022. ���Diversity and Ecological Footprint of Global Ocean RNA Viruses.��� Science 376: 1202���1208.
Enebe, M. C., and M. Erasmus. 2023. ���Vermicomposting Technology ��� A Perspective on Vermicompost Production Technologies Limitations and Prospects.��� Journal of Environmental Management 345: 118585.
Fu, L., B. Niu, Z. Zhu, S. Wu, and W. Li. 2012. ���CD���HIT: Accelerated for Clustering the Next���Generation Sequencing Data.��� Bioinformatics 28: 3150���3152.
Guo, J., B. Bolduc, A. A. Zayed, et al. 2021. ���VirSorter2: A Multi���Classifier, Expert���Guided Approach to Detect Diverse DNA and RNA Viruses.��� Microbiome 9: 37.
Hartmann, M., and J. Six. 2022. ���Soil Structure and Microbiome Functions in Agroecosystems.��� Nature Reviews Earth and Environment 4: 4���18.
Hector, A., and R. Bagchi. 2007. ���Biodiversity and Ecosystem Multifunctionality.��� Nature 448: 188���190.
Hu, W., J. Ran, L. Dong, et al. 2021. ���Aridity���Driven Shift in Biodiversity���Soil Multifunctionality Relationships.��� Nature Communications 12: 5350.
Jaiswal, A. K., Y. Elad, E. Cytryn, E. R. Graber, and O. Frenkel. 2018. ���Activating Biochar by Manipulating the Bacterial and Fungal Microbiome Through Pre���Conditioning.��� New Phytologist 219: 363���377.
Jia, P., J.���L. Liang, J. Lu, et al. 2024. ���Soil Keystone Viruses Are Regulators of Ecosystem Multifunctionality.��� Environment International 191: 108964.
Jin, B.���J., X.���P. Liu, X. L. Roux, et al. 2022. ���Biochar Addition Regulates Soil and Earthworm Gut Microbiome and Multifunctionality.��� Soil Biology and Biochemistry 173: 108810.
Jing, X., N. J. Sanders, Y. Shi, et al. 2015. ���The Links Between Ecosystem Multifunctionality and Above��� and Belowground Biodiversity Are Mediated by Climate.��� Nature Communications 6: 8159.
Johnsen, U., and P. Sch��nheit. 2007. ���Characterization of Cofactor���Dependent and Cofactor���Independent Phosphoglycerate Mutases From Archaea.��� Extremophiles 11: 647���657.
Kieft, K., Z. Zhou, R. E. Anderson, A. Buchan, B. J. Campbell, and S. J. Hallam. 2021. ���Ecology of Inorganic Sulfur Auxiliary Metabolism in Widespread Bacteriophages.��� Nature Communications 12: 3503.
Knowles, B., C. B. Silveira, B. A. Bailey, et al. 2016. ���Lytic to Temperate Switching of Viral Communities.��� Nature 531, no. 7595: 466���470. https://doi.org/10.1038/nature17193.
Li, C., K. Yan, L. Tang, Z. Jia, and Y. Li. 2014. ���Change in Deep Soil Microbial Communities due to Long���Term Fertilization.��� Soil Biology and Biochemistry 75: 264���272.
Li, D., R. Luo, C.���M. Liu, et al. 2016. ���MEGAHIT v1.0: A Fast and Scalable Metagenome Assembler Driven by Advanced Methodologies and Community Practices.��� Methods 102: 3���11.
Li, H., X.���R. Yang, J. Wang, G.���W. Zhou, Y.���S. Zhang, and S. B. Lassen. 2021. ���Earthworm Gut: An Overlooked Niche for Anaerobic Ammonium Oxidation in Agricultural Soil.��� Science of the Total Environment 752: 141874.
Li, J., J. M. Cooper, Z. Lin, Y. Li, X. Yang, and B. Zhao. 2015. ���Soil Microbial Community Structure and Function Are Significantly Affected by Long���Term Organic and Mineral Fertilization Regimes in the North China Plain.��� Applied Soil Ecology 96: 75���87.
Li, J., M. Delgado���Baquerizo, J.���T. Wang, et al. 2019. ���Fungal Richness Contributes to Multifunctionality in Boreal Forest Soil.��� Soil Biology and Biochemistry 136: 107526.
Luo, J., G. Liao, S. Banerjee, et al. 2023. ���Long���Term Organic Fertilization Promotes the Resilience of Soil Multifunctionality Driven by Bacterial Communities.��� Soil Biology and Biochemistry 177: 108922.
Manning, P., F. Van Der Plas, S. Soliveres, et al. 2018. ���Redefining Ecosystem Multifunctionality.��� Nature Ecology & Evolution 2: 427���436.
Maza���M��rquez, P., M. D. Lee, A. M. Detweiler, and B. M. Bebout. 2022. ���Millimeter���Scale Vertical Partitioning of Nitrogen Cycling in Hypersaline Mats Reveals Prominence of Genes Encoding Multi���Heme and Prismane Proteins.��� ISME Journal 16: 1119���1129.
Mazumder, P., A. Pm, K. M. Jyoti, U. Mishra, and A. S. Kalamdhad. 2021. ���Enhancement of Soil Physico���Chemical Properties Post Compost Application: Optimization Using Response Surface Methodology Comprehending Central Composite Design.��� Journal of Environmental Management 289: 112461.
Moriwaki, T., Y. Yamamoto, T. Aida, et al. 2008. ���Overexpression of the Escherichia coli Catalase Gene, katE, Enhances Tolerance to Salinity Stress in the Transgenic Indica Rice Cultivar, BR5.��� Plant Biotechnology Reports 2: 41���46.
Niu, B., J. N. Paulson, X. Zheng, and R. Kolter. 2017. ���Simplified and Representative Bacterial Community of Maize Roots.��� Proceedings of the National Academy of Sciences 114, no. 12: E2450���E2459.
Ogata, H., S. Goto, K. Sato, W. Fujibuchi, H. Bono, and M. Kanehisa. 1999. ���KEGG: Kyoto Encyclopedia of Genes and Genomes.��� Nucleic Acids Research 27: 29���34.
Parastesh, F., H. A. Alikhani, and H. Etesami. 2019. ���Vermicompost Enriched With Phosphate���Solubilizing Bacteria Provides Plant With Enough Phosphorus in a Sequential Cropping Under Calcareous Soil Conditions.��� Journal of Cleaner Production 221: 27���37.
Peng, Y., H. C. M. Leung, S. M. Yiu, and F. Y. L. Chin. 2012. ���IDBA���UD: A De Novo Assembler for Single���Cell and Metagenomic Sequencing Data With Highly Uneven Depth.��� Bioinformatics 28: 1420���1428.
Qiu, L., Q. Zhang, H. Zhu, P. B. Reich, S. Banerjee, and M. G. A. Van Der Heijden. 2021. ���Erosion Reduces Soil Microbial Diversity, Network Complexity and Multifunctionality.��� ISME Journal 15: 2474���2489.
Ren, J., K. Song, C. Deng, et al. 2020. ���Identifying Viruses From Metagenomic Data Using Deep Learning.��� Quantitative Biology 8: 64���77.
Sant, D. G., L. C. Woods, J. J. Barr, and M. J. McDonald. 2021. ���Host Diversity Slows Bacteriophage Adaptation by Selecting Generalists Over Specialists.��� Nature Ecology & Evolution 5: 350���359.
Schuldt, A., T. Assmann, M. Brezzi, F. Buscot, D. Eichenberg, and J. Gutknecht. 2018. ���Biodiversity Across Trophic Levels Drives Multifunctionality in Highly Diverse Forests.��� Nature Communications 9: 2989.
Silveira, C. B., and F. L. Rohwer. 2016. ���Piggyback���The���Winner in Host���Associated Microbial Communities.��� npj Biofilms and Microbiomes 2: 16010.
Tao, C., R. Li, W. Xiong, et al. 2020. ���Bio���Organic Fertilizers Stimulate Indigenous Soil Pseudomonas Populations to Enhance Plant Disease Suppression.��� Microbiome 8: 137.
Tatusov, R. L., N. D. Fedorova, J. D. Jackson, et al. 2003. ���The COG Database: An Updated Version Includes Eukaryotes.��� BMC Bioinformatics 4: 41.
Tong, D., Y. Wang, H. Yu, H. Shen, R. A. Dahlgren, and J. Xu. 2023. ���Viral Lysing Can Alleviate Microbial Nutrient Limitations and Accumulate Recalcitrant Dissolved Organic Matter Components in Soil.��� ISME Journal 17: 1247���1256.
Wagg, C., S. F. Bender, F. Widmer, and M. G. A. Van Der Heijden. 2014. ���Soil Biodiversity and Soil Community Composition Determine Ecosystem Multifunctionality.��� Proceedings of the National Academy of Sciences 111: 5266���5270.
Wang, N., X. Jiang, S. Zhang, et al. 2021. ���Structural Basis of Human Monocarboxylate Transporter 1 Inhibition by Anti���Cancer Drug Candidates.��� Cell 184: 370���383.e13.
Xia, R., M. Sun, J. L. Balc��zar, P. Yu, F. Hu, and P. J. J. Alvarez. 2023. ���Benzo[a]Pyrene Stress Impacts Adaptive Strategies and Ecological Functions of Earthworm Intestinal Viromes.��� ISME Journal 17: 1004���1014.
Yan, L., G. Wang, S. Ai, et al. 2018. ���Abundance of Ammonia���Oxidizing Bacteria and Archaea Under Different Ventilation Strategies During Cattle Manure Composting.��� Journal of Environmental Management 212: 375���383.
Yuan, S., V.���P. Friman, J. L. Balcazar, et al. 2023. ���Viral and Bacterial Communities Collaborate Through Complementary Assembly Processes in Soil to Survive Organochlorine Contamination.��� Applied and Environmental Microbiology 89, no. 3: e01810���22. https://doi.org/10.1128/aem.01810���22.
Zhao, D., H. Chao, J. L. Balcazar, et al. 2024. ���Bacteriophages Assisted Bacteria to Facilitate Soil Multifunctionality Under Organochlorine Pesticide Contamination.��� SCIENCE CHINA Technological Sciences 67, no. 10: 3116���3128. https://doi.org/10.1007/s11431���024���2693���7.
Zhao, S., S. Schmidt, H. Gao, et al. 2022. ���A Precision Compost Strategy Aligning Composts and Application Methods With Target Crops and Growth Environments Can Increase Global Food Production.��� Nature Food 3: 741���752.
Zheng, Q., Y. Hu, S. Zhang, et al. 2019. ���Soil Multifunctionality Is Affected by the Soil Environment and by Microbial Community Composition and Diversity.��� Soil Biology and Biochemistry 136: 107521.
Zheng, X., M. T. Jahn, M. Sun, et al. 2022. ���Organochlorine Contamination Enriches Virus���Encoded Metabolism and Pesticide Degradation Associated Auxiliary Genes in Soil Microbiomes.��� ISME Journal 16, no. 5: 1397���1408. https://doi.org/10.1038/s41396���022���01188���w.
Zhu, W., A. Lomsadze, and M. Borodovsky. 2010. ���Ab Initio Gene Identification In Metagenomic Sequences.��� Nucleic Acids Research 38: e132���e132.
Grants
42077106/National Natural Science Foundation of China
42277115/National Natural Science Foundation of China
Modern Agriculture; BE2022322/Jiangsu Provincial Key Research and Development Program