Fauna-microbe diversity coupling lost in agricultural soils: Implications from the bacteria hidden in earthworm gut

Abstract

Earthworms are critical for supporting soil health and microbial diversity and simultaneously maintaining a highly diverse gut microbiome. The earthworm is predominantly vulnerable to physical disturbance, yet how changes in earthworm diversity influence the richness and ecological network of soil-gut microbiomes in response to anthropogenic disturbance is virtually unknown. Here, we investigated the richness of earthworms, and their connection with the diversity of the soil-gut microbiome using a large-scale survey covering paired agricultural and natural sites. Our results showed that earthworm diversity was positively correlated with soil and gut bacterial diversity across sites. However, the connection between soil bacterial and earthworm diversity is lost in agricultural ecosystems. We further show that earthworm richness supported greater modularity in microbial networks, being both positively correlated with the richness of earthworm gut bacteria in both land-use types. Together, we provided the first empirical evidence that agricultural practices can break the fundamental links between soil bacterial and earthworm diversity, and further identify an unreported consistent connection between the diversity of earthworms and the modularity of microbial networks in natural and managed ecosystems. These findings emphasize the primary roles of earthworms in supporting soil biodiversity and point to the wider contributions of the soil animal-microbe interactions in preserving the whole soil biodiversity in anthropogenically disturbed ecosystems.