Soil microorganisms exhibit enzymatic and priming response to root mucilage under drought

Although root mucilage plays a prominent role in soil-plant-water relations, especially under drought, its persistence in soil and its microbial decomposition remain unknown. The aim of this study was to investigate: 1) the effect of soil moisture on mucilage decomposition, 2) the effect of mucilage on enzyme activities, and 3) the effect of mucilage on soil organic matter (SOM) decomposition. We hypothesized that mucilage benefits soil microorganisms by compensating for the detrimental effects of drought. Consequently, low water content was expected to reduce SOM mineralization and enzyme activities only in soil without mucilage. High moisture was predicted to support high microbial activities and therefore rapid decomposition of the mucilage. Two doses of maize root mucilage (40 and 200 μg C g−1 soil; C4 plant derived) were added to a C3 soil at optimum moisture (80% WHC) and under drought (30% WHC) to test these hypotheses. Under optimum moisture conditions, CO2 efflux from soil increased in proportion to mucilage addition. In contrast, there was no effect of mucilage on CO2 efflux under drought. At 80% WHC, mucilage was nearly completely decomposed (98% and 88% for low and high dose, respectively) after 15 days. Drought significantly suppressed mucilage mineralization. Microbial uptake of mucilage C was independent of soil moisture, suggesting that its bioavailability is regulated not by the water content of the whole soil, but by the water within the swollen mucilage. The high mucilage dose increased microbial biomass at both moisture levels compared to the soil without mucilage. Positive priming of soil organic matter decomposition was induced by mucilage at 80% WHC, whereas at 30% WHC, mucilage caused slightly negative priming. Mucilage addition counteracted the decrease of enzyme activities at 30% WHC, and so, stabilized the catalytic activity irrespective of soil moisture content. We conclude that mucilage provides biofilm-like properties that maintain microbial and exoenzymatic activities, even under drought. The slow decomposition of mucilage in drying soils suggests that mucilage maintains moist conditions around the roots for a long period, supporting beneficial root-microbial interactions at low water availability. This would result in a positive ecological feedback for microbial life in the rhizosphere and enhance nutrient release for roots under water scarcity.