Bt toxins alter bacterial communities and their potential functions in earthworm intestines

Environ Pollut. 2024 Dec 24:125591. doi: 10.1016/j.envpol.2024.125591. Online ahead of print.

Abstract

The accumulation and persistence of Bt toxins in soils from Bt plants and Bt biopesticides can result in ecological hazards. Earthworms are one of the most frequently used bioindicators for soil ecological monitoring, characterization, and risk assessment. However, the effects of Bt toxins on earthworm bacterial communities have conversely rarely been studied. Here, the dynamics of exposure to exogenous Bt toxins in earthworm intestines were investigated alongside the impacts of Bt toxins on intestinal bacterial community diversity, stability, and potential function. The intestinal concentration of water-dissolved Bt toxins drastically decreased with increased incubation time. Intestinal bacterial community compositions in earthworm intestines were affected by the concentration of Bt toxin that was added and incubation time. Moreover, lower bacterial community α diversity (i.e., based on Sobs and ACE indices) and significantly higher predicted relative abundances of microbial enzymes in the Bt toxin treatment compared with the control were observed alongside differences in bacterial taxonomic and functional compositional profiles after Bt toxin exposure. The observed changes were most strongly associated with variation in overall functional redundancy. Intestinal bacterial taxa probably played pivotal roles in the degradation and transformation of Bt toxins via nitrogen, phosphorus, and polysaccharide hydrolysis metabolic pathways. Although the application of Bt toxin led to lower intestinal community α diversity and stability after 14 days, these community characteristics were restored upon further incubation to 21 days. Thus, these results suggest that earthworm intestinal microbial communities confer strong resilience and the ability to adapt to Bt toxin stress. Consequently, persistent adverse effects of Bt toxins on intestinal microbiomes were not observed after earthworm exposure to Bt toxins.

Keywords: 16S rRNA gene sequencing; Bacterial community; Bt toxins; Earthworm intestine; Ecological risks.