Why Bufo gargarizans tadpoles grow bigger in Pb-contaminated environments? The gut microbiota matter

The impacts of lead/Pb²⁺ on ecosystems have received widespread attention. Growth suppression is a major toxic effect of Pb compounds on aquatic animals, however, some studies have also reported their growth-promoting effects. These complex outcomes may be explained by anions that accompany Pb²⁺ or by the multiple toxic mechanisms/pathways of Pb²⁺. To examine these hypotheses, we tested how Bufo gargarizans tadpoles responded to Pb(NO₃)₂ (100 and 200 μg/L Pb²⁺) using transcriptomics and microbiomics, with NaNO₃ and blank groups as controls. Tadpoles exposed to Pb(NO₃)₂ showed delayed development while increased somatic growth in a dose-dependent manner, which can be attributed to the effects of NO₃^- and Pb²⁺, respectively. Tadpole transcriptomics revealed that exposure to NO₃^- downregulated the MAPK pathway at transcriptional level, explaining the development-suppressing effect of NO₃^-; while Pb²⁺ upregulated the transcription of detoxification pathways (e.g., xenobiotics metabolism by cytochrome P450 and glutathione metabolism), indicating cellular stress and thus contradicting the growth advantage of Pb²⁺-exposed tadpoles. Pb²⁺ exposure changed the tadpole gut microbiota drastically, characterized by increased polysaccharides and carbohydrate utilization while decreased fatty acid and amino acid consumption according to microbial functional analysis. Similar gut microbial variations were observed in field-collected tadpoles from different Pb²⁺ environments. This metabolic shift in gut microbiota likely improved the overall food utilization efficiency and increased the allocation of fatty acids and amino acids to the host, explaining the growth advantage of Pb²⁺-exposed tadpoles. In summary, our results suggest multiple toxic pathways of Pb²⁺, and the gut microbiota may affect the pollution outcomes on animals.