Turnover of bacterial biomass to soil organic matter via fungal biomass and its metabolic implications

Microbial biomass residues play a significant role in biogeochemical cycling but the mechanism by which material from microbial sources is sequestered in soil organic matter still remains elusive. Although we previously investigated the detailed turnover process of Gram-negative bacterial biomass (E. coli) derived carbon (C) in soil and found indications that fungi were the first clade to incorporate E. coli-derived C, no reliable estimate is available for the amount of bacterial biomass-derived C that is stabilized via fungal residues during turnover in soils. Here we tracked C-13-amino sugars (from chitin and peptidoglycan) and amino acids (from proteins) in order to shed light onto the bacterial and fungal food web. During incubation, C-13-amino acids decreased significantly, whereas C-13-amino sugars changed only slightly over time, suggesting that amino sugars as biomarkers are relatively stable compared to amino acids. The ratio of C-13-fungal derived glucosamine to C-13-muramic acid significantly increased before day 14, then levelled off until the end of the experiment. This further highlighted that bacterial C was stabilized in soil by conversion to fungal biomass that grew on the bacterial biomass. Interestingly, the shifts in C-13-amino acids distribution pattern reflect three phases of the central metabolism. In the beginning, the added biomass was low in carbohydrates compared to the needs of the active microbes, resulting in a dominance of the glyoxylate cycle. In a second phase, the general metabolism and thus the tricarboxylic acid cycle (TCA) was very active, most probably supported by the use of a mixture of compounds from soil organic matter. This phase also included anaplerotic reactions resulting in C incorporation from CO2. Finally, metabolism slowed down and thus the TCA cycle was less active and C rather than energy was preserved. In summary, our study provided evidence that bacterial biomass residues were predominantly utilized by fungi; thus, at the end, the C was mainly stabilized as fungal necromass. Our results also indicated that bacterial biomass residues were turned over for preservation of C (similar to 50%) rather than energy towards the end of the incubation. This may thus be an important pathway for soil organic carbon sequestration in soil.

Automated summary

Microbial biomass residues play an important role in biogeochemical cycling, but the mechanism by which they are sequestered in soil organic matter remains elusive. This study revealed that bacterial biomass is predominantly utilized by fungi and stabilized as fungal necromass, contributing to soil organic carbon sequestration. The study also identified three phases in the metabolism of microbial biomass residues, with the final phase focused on C preservation rather than energy production.