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 macro aggregates. 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 the face of intensifying anthropogenic land-use and climate change.