Earthworms Facilitate Soil Organic Phosphorus Mineralization Primarily by Their Gut Microbiome

Earthworm gut contains a distinctive bacterial community that actively accelerates nutrient cycling; however, how these bacterial communities regulate soil organic phosphorus (Po) mineralization is still unknown. Here, we investigated the temporal dynamics of different phosphorus (P) fractions and enzyme activities in soil with or without earthworm addition (over 28 days). The absolute phoD gene abundance, phoD-harboring community in the soil and earthworm gut, and lecithin medium-enriched bacterial community were also determined to explore the taxa involved in Po mineralization. Our results show that earthworms increased soil phosphatase activities and NaOH-Po mineralization, and subsequently increased the soil available P content. The phoD-harboring bacterial communities in earthworm-affected soil exhibited a composition similar to that of the earthworm gut, which resulted in a higher Po mineralization capacity in the later stage of incubation. Co-occurrence network analysis showed that earthworms could rapidly increase the complexity and proportion of positive links in the networks of soil phoD-harboring bacterial communities at an early stage. Notably, the phoD-harboring bacterial communities in earthworm gut owned a higher abundance of Burkholderia and higher diversity with stronger Po mineralization capacities. Using Pikovskaya medium, we found that Po mineralization activity was highest in the gut of earthworms during the first two weeks of incubation, but it was highest in earthworm-treated soil in the last stage of incubation. PLS-PM analysis further revealed that the earthworm gut microbiome could promote Po mineralization by directly regulating soil P enzymes and indirectly altering the indicator-keystone taxa of soil phoD-harboring communities including Cellulomonas, Bradyrhizobium, and Pseudomonas. Collectively, our results suggest that the earthworm gut-induced increase in Po mineralization may depend primarily on the strong Po mineralization capacity of their gut microbial community.