Cascading effects of Pb on the environmental and symbiotic microbiota and tadpoles' physiology based on field data and laboratory validation

Abstract

Heavy metal pollution poses a serious threat to ecosystems. Currently, there is a lack of field data that would enable us to gain a systematic understanding of the influences of heavy metals on aquatic ecosystems, especially the interactions between environments and animals. We studied the relationships between the variations in heavy metal concentrations (10 species including Pb in sediments and surface water), the community structure of environmental and symbiotic microbiota, and the gut traits of Bufo gargarizans tadpoles across 16 sampling sites on the Chengdu Plain through rigorous statistical analysis and laboratory validation. The results show that heavy metal concentrations, especially the Pb concentration of the sediment, are linked to the variations in sediment and tadpoles' gut microbiomes but not to water microbiota. For the sediment microbiota, Pb causes a trade-off between the proportions of Burkholderiales and Verrucomicrobiae and affects the methane, sulfide, and nitrate metabolisms. For tadpoles, a high sediment Pb content leads to a low abundance of gut aerobic bacteria and a large relative gut weight under both field and laboratory conditions. In addition, Pb promotes the growth of B. gargarizans tadpoles under laboratory conditions. These effects seem to be beneficial to tadpoles. However, a high Pb content leads to a low abundance of probiotic bacteria (e.g., Verrucomicrobiae, Eubacteriaceae, and Cetobacterium) and a high abundance of pathogenic bacteria in the gut and environment, suggesting potential health risks posed by Pb. Interestingly, there is a causal relationship between Pb-induced variations in sediment and symbiotic microbiotas, and the latter is further linked to the variation in relative gut weight of tadpoles. This suggests a cascading effect of Pb on the ecosystem. In conclusion, our results indicate that among the heavy metals, the Pb in sediment is a critical factor affecting the aquatic ecosystem through an environment-gut-physiology pathway mediated by microbiota.