The booming intensive agriculture decreases soil protistan diversity and multifunctionality

Protists are crucial in regulating soil microbiome and providing various ecosystem services, establishing themselves as key entities in soils. The booming intensive agriculture contributes significantly to the increasing global demand for plentiful and diverse food. However, the changes of soil protistan communities during the transition from traditional open field (OF) to intensive plastic shed (PS) cultivation systems, along with their impact on soil multifunctionality, remain poorly understood. In this study, 396 pairwise OF and PS soils were collected from 89 sites across China. Soil protistan communities and multifunctionality were analyzed using 18S rRNA gene amplicon and metagenomics sequencing. The findings revealed that PS led to a significant decrease in alpha-diversity and habitat niche breadth of rare protists, while increasing those of abundant protists compared to OF. The protistan communities were less constrained by geographical distance and soil properties in the PS. Climatic factors emerged as the primary predictors of protistan communities in both OF and PS soils. High latitude regions exhibited greater dissimilarities in the phagotrophic protistan community between paired OF and PS soils. The soil multifunctionality index was notably lower in the PS soils than in the OF soils, with the phylogenetic diversity and community structure of rare protists playing a pivotal role in determining soil multifunctionality. An independent experiment demonstrated that the inoculation of rare protistan community from local OF soils significantly enhanced the microbial eco-functions of the PS soils. To our knowledge, this study first underscores the significance of rare protists in soil multifunctionality and emphasizes the importance of preserving these rare taxa in supporting the sustainable development of intensive agriculture.