Soil organic carbon loss decreases biodiversity but stimulates multitrophic interactions that promote belowground metabolism

Soil organic carbon (SOC) plays an essential role in mediating community structure and metabolic activities of belowground biota. Unraveling the evolution of belowground communities and their feedback mechanisms on SOC dynamics helps embed the ecology of soil microbiome into carbon cycling, which serves to improve biodiversity conservation and carbon management strategy under global change. Here, croplands with a SOC gradient were used to understand how belowground metabolisms and SOC decomposition were linked to the diversity, composition, and co-occurrence networks of belowground communities encompassing archaea, bacteria, fungi, protists, and invertebrates. As SOC decreased, the diversity of prokaryotes and eukaryotes also decreased, but their network complexity showed contrasting patterns: prokaryotes increased due to intensified niche overlap, while that of eukaryotes decreased possibly because of greater dispersal limitation owing to the breakdown of macroaggregates. Despite the decrease in biodiversity and SOC stocks, the belowground metabolic capacity was enhanced as indicated by increased enzyme activity and decreased enzymatic stoichiometric imbalance. This could, in turn, expedite carbon loss through respiration, particularly in the slow-cycling pool. The enhanced belowground metabolic capacity was dominantly driven by greater multitrophic network complexity and particularly negative (competitive and predator-prey) associations, which fostered the stability of the belowground metacommunity. Interestingly, soil abiotic conditions including pH, aeration, and nutrient stocks, exhibited a less significant role. Overall, this study reveals a greater need for soil C resources across multitrophic levels to maintain metabolic functionality as declining SOC results in biodiversity loss. Our researchers highlight the importance of integrating belowground biological processes into models of SOC turnover, to improve agroecosystem functioning and carbon management in face of intensifying anthropogenic land-use and climate change. A conceptual diagram illustrating that the belowground metacommunity strengthens metabolic capacity in response to decreased resource availability by forming a more complex and competitive multitrophic network. Under SOC decline, the belowground biota are stimulated to generate more multitrophic interactions especially negative associations, with the purpose of more efficiently acquiring carbon and energy. Consequently, despite of the decreases in biodiversity and SOC content, the enhanced enzyme activities and reduced enzymatic stoichiometric imbalance accelerate the carbon loss especially in the slow-cycling pool.image