Effect of phenanthrene on the biological characteristics of earthworm casts and their relationships with digestive and anti-oxidative systems

Abstract

Earthworms as ecosystem engineers partially improve soil properties by egesting casts. Our previous study confirmed that soil pollution affects the physico-chemical properties of earthworm casts. It is still unclear whether the biological properties (e.g. cellulase, urease, and acid and alkaline phosphatase activities, as well as microbial biomass carbon) of casts are affected by foreign substances in soil. The present study aimed to investigate the effect of phenanthrene (PHE) on the biological characteristics of earthworm (Eisenia fetida) casts. Furthermore, correlations between cast properties and the digestive and antioxidant systems were explored by the determination of digestive enzyme (urease, protease, acid and alkaline phosphatase) activities, antioxidant indexes [superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD)], as well as malondialdehyde (MDA) content. Exposure at a range of PHE doses (0, 2, 5, 10, and 20 mg kg^-1) for 15 d resulted in the following observations: (1) Compared with urease, as well as acid and alkaline phosphatase activities, cellulase activities in both soil and casts were sensitive to PHE, and could potentially act as biomarkers to provide early-warning signals for soil pollution. (2) Microbial biomass carbon in casts was modified, but with no clear pattern. (3) Cellulase and POD activities, as well as MDA content in earthworms, increased with elevated exposure to PHE in soil. Protease, SOD, and CAT activities exhibited a biphasic dose response to PHE, while acid and alkaline phosphatase activities were inhibited under treatment conditions. (4) Correlation analysis suggested that microbial biomass carbon in casts significantly and positively correlated with cellulase and acid phosphatase activities of earthworms, but negatively correlated with protease activities. A significant but weak negative correlation between alkaline phosphatase activities in casts and POD activities was also observed. Based on these results, we concluded that PHE content in soil modified some biological properties of casts, by partially affecting the earthworm's digestive and antioxidant systems. This study advances our knowledge of earthworm ecology in polluted soil by providing a better understanding of their ecological functions.

Keywords: Digestive enzyme; Earthworm casts; Malondialdehyde (MDA); Microbial biomass carbon (MBC); Polycyclic aromatic hydrocarbons (PAHs); Superoxide dismutase (SOD).