Organic fertilization drives shifts in microbiome complexity and keystone taxa increase the resistance of microbial mediated functions to biodiversity loss

Long-term intensive fertilization profoundly alters soil properties including microbial diversity and co-occurrence associations, but little is known about the relative and combined importance of biotic and abiotic factors for the stability of soil microbial mediated functions (MMF) to biodiversity loss. Here, we experimentally manipulated microbial alpha-diversity by inoculating diluted soil suspensions into sterilized soil to tease apart the biotic and abiotic effects on the microbiomes and temporal shifts in MMF in soils subjected to different fertilization treatments during a 3-month re-colonization. We showed that bacterial and fungal biomass remained similar between different diversity levels at each sampling date (0, 7, 15, 30, and 90 days). Organic fertilization accelerated the resilience of copiotrophic bacterial assemblages to biodiversity loss compared with non-fertilization and mineral fertilization and increased the strength of positive relationships between soil MMF and diversity and network complexity of bacterial rather than fungal community. A suite of biotic and abiotic factors were found to account for up to 73% of the variation in MMF, with the combined effects of diversity and microbiome complexity accounting for 43% of the variation in MMF. Moreover, the overall diversity of keystone taxa, primarily driven by soil organic carbon, was particularly important for promoting soil MMF (P < 0.001), with the abundances of oligotrophic- (Blastocatellaceae) and copiotrophic-selected (Comamonadaceae) keystone taxa positively and negatively relating to soil MMF, respectively. Collectively, our study indicates the importance of fertilization-induced shifts in network complexity and microbial life strategies for maintaining the stability of MMF following biodiversity decline and calls for organically based microbiome complexity conservation strategies to mitigate negative impacts of biodiversity loss on multiple agroecosystem functions.

Automated summary

Long-term intensive fertilization can greatly alter soil properties and microbial diversity. In this study, we manipulated microbial alpha-diversity to investigate the effects of biotic and abiotic factors on soil microbial mediated functions (MMF). We found that organic fertilization enhanced the resilience of bacterial assemblages to biodiversity loss and increased the positive relationship between soil MMF and bacterial diversity. Factors including diversity and microbiome complexity accounted for 43% of the variation in MMF. Our study highlights the importance of fertilization-induced shifts in network complexity and microbial life strategies for maintaining stable MMF and suggests the need for organically based strategies to mitigate the negative impacts of biodiversity loss on agroecosystem functions.