Tungsten in Agricultural Soil Triggers Coordinated Bioenergetic Responses and Gut Microbiome Dysbiosis in Earthworms: Implications for Agricultural Soil Health

Abstract

Tungsten (W) can accumulate in agricultural soils near mining, smelting, industrial, and waste-disposal sites, yet its chronic effects on beneficial soil fauna remain poorly understood. Eisenia fetida were exposed for 28 d to soil W concentrations selected with reference to agricultural contamination and toxicity assessment. Despite minimal mortality, W caused concentration-dependent growth inhibition and pronounced reproductive toxicity, with cocoon production declining by 76.4% at 700 mg kg–1 and being completely inhibited at 1500 mg kg–1. Integrated biochemical, histopathological, transcriptomic, metabolomic, and gut microbiome analyses revealed coordinated responses centered on bioenergetic constraint. Internal W accumulation disrupted redox homeostasis, glutathione-dependent detoxification, mitochondrial energy metabolism, and sulfur metabolism, resulting in ATP depletion, Ca2+ dysregulation, acetylcholinesterase inhibition, and tissue injury. W also induced marked gut microbiome dysbiosis. Procrustes and DIABLO analyses supported coordinated responses across omics layers. These findings support a proposed mechanistic framework in which bioenergetic constraint represents an important component of W-associated physiological dysfunction and reproductive impairment in earthworms.