Microbial community regulation of extracellular enzyme production can mediate patterns of particulate and mineral-associated organic matter accumulation in undersaturated soils

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Abstract

Dissolved low molecular weight (LMW) compounds in soil can either be assimilated by microbes or sorb onto mineral surfaces, forming mineral-associated organic matter (MAOM). This creates potential ‘competition’ between microbes and mineral surfaces for LMW compounds, potentially influencing whether particulate organic matter (POM) is retained or depolymerized by microbes to produce LMW substrates. Therefore, microscale interactions between unoccupied mineral surfaces and microbial enzymes may mediate patterns of POM and MAOM storage, particularly in soils varying in MAOM saturation. To explore this, we adapted an individual-based microscale model to simulate POM retention and new MAOM formation under different initial POM qualities (carbon:nitrogen ratio; C:N) and MAOM saturation levels, while also considering microbial social-like dynamics, which emerge from interactions between microbes with different capacities to produce and share public goods (in this case, extracellular enzymes). Consistent with prior findings, the presence of these dynamics slowed decomposition of initial POM pools. Additionally, MAOM saturation affected microbial community properties, new MAOM formation, and POM decomposition only when social dynamics were included. The patterns of POM decomposition and MAOM formation identified in our work align with observations of simultaneous POM and MAOM formation in undersaturated soils from prior field studies, suggesting that regulation of enzyme production via microbial interactions may be an additional driver of POM and MAOM storage in such soils. Overall, this highlights the importance of explicitly incorporating microbial ecology into our conceptual understanding of C and N cycling, particularly to improve the predictive capacity of ecosystem models and inform soil management strategies that enhance global change mitigation, especially in degraded soils likely to be undersaturated.

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