Did Application of Digested Sewage Sludge as Soil Amendment Alter the Abundances of Antibiotic Resistance Genes and Microbial Communities in Soil and Earthworm Gut?

Abstract Background Digested sewage sludge has been widely applied as soil amendment for enhanced crop production. However, given that digested sludge is abundant with antibiotic resistance genes (ARGs) and antibiotic resistant bacteria, the impact of digested sludge amendment on the abundances of ARGs and microbial communities in soil and soil fauna (e.g., earthworms) remains largely unknown. In this study, the patterns of ARGs and microbial communities in soil and gut of earthworms after 80-days cultivation with digested sewage sludge amendment were investigated to gain insights into this impact. Results The results show that the digested sludge amendment increased the initial abundances of ARGs (e.g., tetA, tetQ, and sulII) in soil. However, after 80-days cultivation, the absolute abundances of target ARGs decreased by 62.3–95.4%. The reduction in ARGs absolute abundances was further enhanced by 31.4–84.7% in the presence of earthworms. In contrast, the relative abundances of some ARGs (e.g., tetA, sulI, and blaTEM−1) in the gut of earthworms increased by 41–130 folds. The microbial community structure of soil was greatly altered because of the introduction of digested sewage sludge at initial, but it recovered to its original pattern after 80-days cultivation. This could be attributed to the gradual attenuation of anaerobic microorganisms under aerobic conditions in soil. In particular, the presence of earthworms further enhanced this phenomenon. The reduction of ARGs in the amended soils was likely attributed to microbial community shift based on redundancy analysis. Several bacterial families (e.g., Saprospiraceae, Chitinophagaceae, and Rhodanobacteraceae) were significantly correlated with the target ARGs. Conclusions Our results reveal that the enrichment of ARGs in soil caused by digested sludge-amendment would recover to their original levels before amendment, highlighting the contribution of earthworms to reducing the ARG abundances in amended soil via shifting the microbial community. However, we also found that the amended soil could increase ARGs abundance in the earthworm gut, which may enhance the potential risk of ARGs spread via food chain. These results may provide a new sight on the control of ARGs occurrence and dissemination in sludge-amended soil ecosystem with consideration of the impact of earthworms.