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

Microbial biomass is increasingly considered to be the main source of organic carbon (C) sequestration in soils. Quantitative information on the contribution of microbial necromass to soil organic carbon (SOC) formation and the factors driving necromass accumulation, decomposition and stabilization during the initial soil formation in biological crusts (biocrusts) is absent. 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, 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 in soil was analyzed based on amino sugars -the cell wall biomarker. 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 remained more in the particulate organic C (POC). MAOC pool was saturated fast with the increase of microbial necromass, and POC more rapid accumulation than MAOC suggests that the clay content was the limiting factor for stable C accumulation in this sandy soil. The necromass exceeding the MAOC stabilization level was stored in the labile POC pool (especially necromass from fungi). Activities of four enzymes (i.e., beta-1,4-glucosidase, beta-1,4-N-acetyl-glucosaminidase, leucine aminopeptidase, and alkaline phosphatase) increasing with fungal and bacterial necromass suggest that the raised activity of living microorganisms accelerated the turnover and formation of necromass. Microbial N limitation raised the production of N acquisition enzymes (e.g., beta-1,4-N-acetyl-glucosaminidase and leucine aminopeptidase) to break down necromass compounds, leading to further increase of the nutrient pool in soil solution. The decrease of microbial N limitation along the biocrusts formation chronosequence is an important factor for the necromass accumulation during initial soil development. High microbial N demands and insufficient clay protection lead to fast necromass reutilization by microorganisms and thus, result 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 biocrust is lower (12-25%) than in fully developed soils (33%- 60%, literature data). Nitrogen (N) limitation of microorganisms and an increased ratio between N-acquiring enzyme activities and microbial N, as well as limited clay protection, resulted in a low contribution of microbial necromass to SOC by initial formation of biocrust-covered sandy soil. Summarizing, soil development leads not only to SOC accumulation, but also to increased contribution of microbial necromass to SOC, whereas the plant litter contribution decreases