Modeling microbial regulatory feedback in organic matter decomposition identifies copiotrophic traits as key drivers of positive priming

Microbial decomposition of complex soil organic matter (OM) is often regulated by labile organic carbon inputs, a phenomenon known as priming, which plays a critical role in belowground biogeochemical cycling. However, the strength and direction of microbial priming of soil OM pools varies significantly across ecosystems. A generalizable mechanistic framework explaining the factors that lead to accelerated (positive priming) or impeded (negative priming) rates of OM decomposition is still lacking. In this work, we conceptualize priming as a microbial feedback loop that optimizes the costs and benefits of maximizing growth rate, specifically, the cost of exoenzyme synthesis for decomposing complex OM versus the benefit of energy acquisition from labile OM. We examined the impacts of microbial functional traits and interactions on priming by employing a cybernetic modelling approach, which predicts complex microbial growth patterns by accounting for dynamic metabolic regulations. We simulated microbial priming across ecological community configurations composed of degraders and non-degraders with either oligotrophic or copiotrophic traits, resulting in seven combinations that included both single functional groups (degraders with either trophic trait) and binary functional groups (combinations of degraders and non-degraders, or degraders only, with differing or common trophic traits). Configurations with only non-degraders were excluded, as they are irrelevant for studying priming in OM decomposition. Monte Carlo simulations for these scenarios revealed: (1) positive priming is prevalent, while negative priming occurs sporadically under specific parameter settings; (2) positive priming is more frequently observed in microbial systems with copiotrophic degraders than those with oligotrophic degraders; (3) the presence of copiotrophic non-degraders suppresses positive priming, whereas the presence of oligotrophic non-degraders promotes it; and (4) the temporal dynamics of priming is also influenced by microbial functional traits and interactions. These findings highlight the driving role of microbial functional traits and interactions in priming. Notably, copiotrophic degraders inducing strong positive priming is consistent with microbial energy mining through enhanced degradation of complex OM, whereas suppression of positive priming under copiotrophic non-degraders suggests reduced use of labile OM for co-metabolism and complex OM-degrading enzyme production. Most strikingly, our simulations predicted a dramatic positive priming effect triggered by the addition of a small amount of labile OM (i.e., specifically less than 10 % of the total OM in the complex and labile OM mixture in this study), with no notable changes observed beyond this point. This indicates that microbial regulatory feedback operates nonlinearly, possibly reflecting saturation of microbial demand for energy. As we used a generalized microbial model, we hypothesize that our findings may reflect common features of OM priming across diverse microbial systems and environments. Overall, this work, combining new theories and models, significantly enhances our understanding of priming by providing model-generated and empirically testable hypotheses on the mechanisms governing it.