Control of Soil Extracellular Enzyme Activities by Clay Minerals—Perspectives on Microbial Responses

Abstract

Knowledge of how interactions of clay minerals and extracellular enzymes (EEs) influence organic matter turnover in soils are still under discussion. We studied the effect of different montmorillonite contents on EE activities, using two experiments—(1) an adsorption experiment with a commercially available enzyme (α-glucosidase) and (2) an incubation experiment (10 days) where microorganisms were stimulated to produce enzymes through organic carbon (OC) addition (starch and cellulose). Soil mixtures with different montmorillonite contents were created in four levels to a sandy soil: +0% (control), +0.1%, +1%, and +10%. The potential enzyme activity (pEA) of four enzymes, α-glucosidase, β-glucosidase, cellobiohydrolase, and aminopeptidase, involved in the soil carbon and nitrogen cycle were analysed. The adsorption experiment revealed a reduction in the catalytic activity of α-glucosidase by up to 76% with increasing montmorillonite contents. However, the incubation experiment showed an inhibitory effect on pEA only directly after the stimulation of in-situ EE production by OC addition. At later incubation stages, higher pEA was found in soils with higher montmorillonite contents. This mismatch between both experiments, with a transient reduction in catalytic activity for the incubation experiments, points to the continuous production of enzymes by soil microorganisms. It is conceivable that microbial adaptation is characterized by higher investment in EEs production induced by increasing clay contents and a stabilisation of the EEs by clay minerals. Our results point to the need to better understand EE-clay mineral-OC interactions regarding potential microbial adaptations and EE stabilisation with potentially prolonged activities.

Persistent Activities of Extracellular Enzymes Adsorbed to Soil Minerals

“…Nonetheless, we found the specific activities of the adsorbed enzymes to be higher than those of the free enzymes immediately after adsorption ( Figure 2 ) and throughout the entire study period ( Figure S3 ). This is in contrast to common findings of reduced activities upon enzyme adsorption to minerals [ 9 , 10 , 39 ], although most studies report potential rather than specific enzyme activities. Nevertheless, our observation aligns with the result of Giaveno et al [ 40 ], who reported a 20% increase in potential phytase activity upon adsorption to hematite.…”

“…However, we did not find a universal relationship between the availability of adsorption sites, the adsorption of enzymes, their specific activity, and persistence, which is applicable for different types of minerals. Nevertheless, the presumed reduction in enzyme activities due to adsorption in soils [ 9 , 10 , 38 ] may not always hold true, as the effect on each enzyme likely varies with mineral types, as well as enzymes and the respective sorption-site density provided on the mineral surfaces. Additionally, soil minerals may regulate persistence of extracellular enzymes in soil by, e.g., protection from proteolytic enzymes and direct microbial attack; however, such evidence has mostly been tested over short periods, such as 24 h [ 17 , 44 ].…”

“…We used a sandy soil collected from a research site located at Eberswalde-Müncheberg, Germany (52°30′55.0″ N 14°07′40.5″ E). Soil characteristics have been described in detail in Olagoke et al [ 10 ]. The soil was selected for its low clay content (40 g kg −1 ), and it has a pH of 5.9.…”

“…We applied the generalized linear model (GLM), as described by Olagoke et al [ 10 ]. The pure soil treatment (control) was used as reference for analyses of changes in specific enzyme activities over time.…”

“…In a free state, they are likely subjected to rapid denaturation or enzymatic degradation [ 6 ]. Adsorption to soil minerals is assumed to protect enzymes against degradation [ 7 ] and to modify their activities [ 8 , 9 , 10 ]. However, the persistence of the activity of adsorbed enzymes remains poorly understood.…”