Fungal key players of cellulose utilization: Microbial networks in aggregates of long-term fertilized soils disentangled using 13C-DNA-stable isotope probing

Abstract

Long-term compost application accelerates organic carbon (C) accumulation and macroaggregate formation in soil. Stable aggregates and high soil organic C (SOC) content are supposed to increase microbiota activity and promote transformation of litter compounds (i.e., cellulose) into SOC. Here, we used 13C-DNA-stable isotope probing with subsequent high-throughput sequencing to characterize fungal succession and co-occurrence trends during 13C-cellulose decomposition in aggregate size classes in soils subjected to no fertilizer (control), nitrogen‐phosphorus‑potassium (NPK) fertilizers, and compost (Compost) application for 27 years. Ascomycota (mostly saprotrophic fungi) were always highly competitive for cellulose in all aggregate size classes at the early stages of cellulose decomposition (20 days). Compost-treated soil was enriched with Ascomycota compared to the control soil, wherein Sordariomycetes, the majority, strongly dominated the cellulose utilization (13C incorporation in DNA). 13C-labeled fungal communities converged in the Compost soil, with lower abundance and diversity compared with the NPK and control soils. Such convergence led to greater cellulose decomposition, indicating that compost amendment increased the capacity of a few dominant fungal taxa to decompose litter. Compost soil had more 13C-labeled fungal decomposers in microaggregates and lower fungal decomposers in macroaggregates when compared with the levels in the NPK and control soils. This implies that compost application facilitates fungal colonization towards smaller aggregates. Fungal interactions were reinforced in microaggregates (<250 μm), with more positive associations than those in macroaggregates (>250 μm), indicating greater fungal synergism for recalcitrant resource utilization in microaggregates. The keystone taxa in the co-occurrence networks were not related to cellulose decomposition in microaggregates, but did in macroaggregates. The findings advance a process-based understanding of cellulose utilization by fungal key players based on C and energy availability and the regulation of microbial activity at the aggregate level.