Initial soil formation by biocrusts: nitrogen demand and clay protection control microbial necromass accrual and recycling

Microbial biomass and necromass are increasingly considered to be the main source of organic carbon (C) formation in soils. However, quantitative information on the contribution of microbial necromass to soil organic carbon (SOC) formation and the factors driving microbial necromass accumulation, decomposition and stabilization during initial soil formation in biological crusts (biocrusts) have remained elusive. To address this knowledge gap, we investigated the composition of microbial necromass and its contributions to SOC sequestration in a biocrust formation sequence consisting of five stages: bare sand stage, cyanobacteria stage, cyanobacteria-moss stage, moss-cyanobacteria stage, and moss stage on sandy parent material on the Loess Plateau. The fungal and bacterial necromass C content was analyzed based on cell wall biomarkers, i.e. amino sugars. Microbial necromass was an important source of SOC, and was incorporated into the particulate and mineral-associated organic C (MAOC). Because bacteria have smaller and thinner cell wall fragments as well as more proteins than fungi, bacterial necromass mainly contributed to the MAOC pool, while fungal residues contributed more to the particulate organic C (POC) pool. MAOC saturation by microbial necromass and the fact that POC accumulated more rapidly than MAOC during initial soil formation suggest that the clay content was the limiting factor for stable C accumulation in this sandy soil. Microbial necromass exceeding the MAOC saturation level was further stored in the labile POC pool (especially necromass from fungi). Activities of four enzymes (i.e., β-1,4-glucosidase, β-1,4-N-acetyl-glucosaminidase, leucine aminopeptidase, and alkaline phosphatase) increased with fungal and bacterial necromass, suggesting that the increasing activity of living microorganisms led to an accelerated turnover and formation of necromass. Microbial N limitation raised the production of N acquisition enzymes (e.g., β-1,4-N-acetyl-glucosaminidase and leucine aminopeptidase) to break down necromass compounds, leading to further increases of bio-available N in soil solution. The decrease of microbial N limitation along the biocrust formation chronosequence is an important factor triggering microbial necromass accumulation during initial soil development. High microbial N demands and insufficient clay protection led to fast necromass reutilization by microorganisms and thus, resulted in a low necromass accumulation coefficient, that is, the ratio of microbial necromass to living microbial biomass (on average, 9.6). Consequently, microbial necromass contribution to SOC during initial soil formation by biocrusts was lower (12-25%) than commonly found in fully developed soils (33%-60%, literature data). Nitrogen limitation of microorganisms and increased ratios between N-acquiring enzyme activities and microbial biomass N, as well as limited clay protection and MAOC saturation resulted in a low contribution of microbial necromass to SOC during initial development of this biocrust-covered sandy soil. in summary, soil development led not only to SOC accumulation, but also to increased contribution of microbial necromass to SOC, while the plant biomass contribution to SOC decreased.