Microbial keystone taxa drive crop productivity through shifting aboveground-belowground mineral element flows

Unbalanced fertilization of nutritional elements is a potential threat to environmental quality and agricultural productivity in acid soil. Harnessing keystone taxa in soil microbiome represents a promising strategy to enhance crop productivity as well as reducing the adverse environmental effects of fertilizers, with the goal of agricultural sustainability. However, there is a lack of information on which and how soil microbial keystone taxa contribute to sustainable crop productivity in acid soil. Here, we examined soil microbial communities (including bacteria, fungi, and archaea) and soil nutrients, and the mineral nutrition and yield of maize subjected to different inorganic and organic fertilization treatments over 35 years in acid soil. The application of organic fertilizer alone or in combination with inorganic fertilizers sustained high maize yield when compared with the other fertilization treatments. Microbial abundances and community structures rather than their alpha diversities explained the main variation in maize yield among different treatments. Sixteen soil keystone taxa (a fungal operational taxonomic unit and 15 bacterial operational taxonomic units) were identified from the microbial co-occurrence network. Among them, five keystone taxa (in Hypocreales, Bryobacter, Solirubrobacterales, Thermomicrobiales, and Roseiflexaceae) contributed to high maize yield through increasing phosphorus flow and inhibiting toxic aluminum and manganese flow from soils to plants. However, the remaining eleven keystone taxa (in Conexibacter, Acidothermus, Ktedonobacteraceae, Deltaproteobacteria, Actinobacteria, Elsterales, Ktedonobacterales, and WPS-2) exerted the opposite effects. As a result, maize productivity varied among different fertilization treatments because of the altered maize mineral element flows by microbial keystone taxa. We conclude that microbial keystone taxa drive crop productivity through shifting aboveground-belowground mineral element flows in acid soil. This study highlights the importance of microbial keystone taxa for sustainable crop productivity in acid soil and provides deep insights into the relationships between soil microbial keystone taxa, crop mineral nutrition, and productivity.