Heavy metal contamination collapses trophic interactions in the soil microbial food web via bottom-up regulation

The soil microbial food web plays a vital role in soil health, nutrient cycling and agricultural productivity. Notably, there is a distinct paucity of information regarding the effects of heavy metal contamination on trophic-level interactions within the microbial food web of agricultural soils, which experience appreciably metal contamination worldwide. Herein, we investigated trophic interactions among predators (protists), their preys (bacteria and fungi) and competitors (nematodes) under four metal contamination levels using high-throughput sequencing and a laboratory verification experiment. Metal contamination decreased growth of protist-preferential prey (e.g., small-sized and gram-negative bacteria), increased the growth of protist-nonpreferential prey (e.g., pathogenic fungi and Actinobacteria), and had a limited effect on the soil protist-competitor (i.e., nematodes). This resulted in a considerable decrease in the diversity and abundance of protistan consumers and a re-arrangement of their interactions with other organisms. From a systemic view, the direct link was weaker between heavy metal contamination and the protist community than the indirect linkage, i.e., metal-induced changes in the prey community. We further validated these results with laboratory incubation trials that documented growth inhibition of protist (Colpoda) and protist-preferential prey (Spingomonas) versus growth stimulation of protist-nonpreferential prey (Arthrobacter) under metal contamination. These findings indicate that metal contamination collapses trophic-level interactions within the soil microbial food web via bottom-up regulation, providing important implications for managing trophic interactions to maintain agricultural ecosystem services under the challenge of worldwide metal contamination.