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Microbial transformations of extraneous substrates and soil carbon sequestration

Microbial transformation pattern of labile carbon

Substrate availability not only affects microbial community structure and enzymatic response, but also affects microbial utilization efficiency of substrates, thus determining the accumulation of microbial residues and metabolites in the soil. As important constituents of microbial cell walls, amino sugars are considered to be a storage pool for both the immobilized N and stable soil organic carbon. Hence their dynamics largely depends on the status of carbon and nitrogen in the soil. Amino sugars are reliable microbial residue biomarkers due to their different origins. Among the identified amino sugars, muramic acid (MurN) originates exclusively from bacteria, being a component of the peptidoglycan in the bacterial cell wall. Glucosamine (GluN) in soil occurs mainly in the form of chitin in fungal cell walls. Amino sugars in the soil are contained primarily in dead microbial residue derived from living biomass. They may thus reflect current and historical changes in microorganism community structure. When 13C-labeled labile substrate (e.g., glucose, etc.) are assimilated by microorganisms and involved in metabolic processes, portions of 13C are transformed into amino sugars, amino acid enantiomers and microbial residues. Thus the 13C enrichment (APE) increases rapidly. The 13C enrichment of each amino sugar in soil remained significantly higher than that of black soil during the entire incubation, suggesting more efficient utilization of extraneous substrates in soil with lower SOM and microbial activity. Microorganisms suffering starvation were found to utilize labile substrates for metabolism. This kind of rapid response of microorganisms to capture the available substrate is an important driving force for the immobilization of extraneous carbon inputs.

13C enrichments in different amino sugars were fitted to hyperbolic equations and explicitly reflect the temporal response of different microbial populations to the substrates. The compound-specific pattern of isotope incorporation, i.e., the different dynamics of 13C enrichment for MurN and GluN, suggested that bacteria were initially more competitive than fungi in assimilating a simple substrate, while fungi were dominant in the late stages of organic matter decomposition, causing temporal dynamic changes in bacteria and fungal communities. The APE peak of MurN and fungal-derived GlcN represented the maximal extent of bacterial and fungal populations, respectively, and their ability to become active in response to the available substrates. Furthermore, the dynamics of labeled and unlabeled portions of amino sugars were compound-specific and substrate-dependent, suggesting their different stability in soils. GluN tended to accumulate in soil while MurN was more likely to be degraded as a carbon source when the supply of nitrogen was excessive.

Figure 23: 13C enrichment in amino sugars during incubation

B: black soil       R: Red soil

MurN: muramic acid; GluN: glucosamine; GalN: galactosamine

 

As incubation progressed, a new equilibrium was approached, including the succession between bacteria and fungi, the growth and mortality of organisms, the synthesis of new compounds and the decomposition of organic residues. Even in the case of a continuous supply of labile substrate, a significant substrate saturation point was observed during microbial assimilation of extraneous substrates. The 13C enrichment of each amino sugar in soil with low organic matter (e.g., red soil) was significantly higher than that in soil with high organic matter content (e.g., black soil), indicating that starvation not only stimulates the continual microbial assimilation of available carbon, but also significantly promotes the transformation and renewal of soil organic components.

The adaptive succession and strategies of soil microorganisms

In order to elucidate the kinetics of residue-derived amino sugar formation, we set up a microcosm experiment with agricultural topsoil under two distinct tillage management regimes (conventional tillage, CT; no-till, NT) and uniformly 13C-labeled wheat residues from different plant parts (grain, leaf and root) over a 21-day incubation period. LC-IRMS techniques were used to measure the isotopic composition of individual amino sugars.

After the addition of 13C-labelled plant materials, the muramic acid incorporated a low proportion of exogenous carbon. The residue-derived glucosamine formation could be simulated with a first-order kinetic model. These results suggested that soil fungi outperformed bacteria in efficiently incorporating the organic substrates (Figure 24). Furthermore, the abundance of 13C-glucosamine was ranked in the order of grain > leaf > root, which agreed with the order of residue quality. Such effects on residue quality suggested that it was the availability of carbon that determined the fungal assimilation capacity of the above added substrates. Compared to soils with high organic matter (e.g. no-till, NT), fungi displayed a greater capability of utilizing available high labile C than soils with low organic matter content. In contrast, in the leaf and root treatments, the abundance of 13C-glucosamine was lower in CT than in NT. Thus, less readily available substrates proved to be unfavorable to fungal development, due most likely to the adaptive strategies of energy capture and metabolism. This study was the first to utilize a first-order kinetic model to describe the formation processes of residue-derived amino sugars, in the processes providing microbial succession footprints as affected by both substrate quality and tillage histories.

 

Figure 24: Residue-derived amino sugar concentrations as a function of time

£Grain ™Leaf sRoot







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