Biological transfer of dietary lead in relation to 15N fractionation and the gut microbiome in a soil collembolan-predatory mite food chain

W.C. Daia, b, Zhu Lia, X. Kec, Y.M. Luoa, P. Christiea and L. H. Wua

a Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences

b College of Resources and Environment, Southwest University

c Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences

Presenting author, E-mail: lizhu@issas.ac.cn

Abstract: Lead (Pb) pollution is a global environmental problem that results in ecological and human health risks. Effects of Pb on single species of collembolans and predatory mites have been studied in some detail but Pb accumulation and biological transfer and the relationship between Pb trophic transfer and nitrogen isotope fractionation and changes in the gut microbiome through soil micro-arthropod food chains remain poorly understood. A plate system experiment was conducted to investigate the biological transfer and trophic toxicity of Pb and the effects of dietary Pb exposure on 15N in animal tissues and changes in the gut microbiome in a soil collembolan (Folsomia candida) – predatory mite (Hypoaspis aculeifer) food chain. Thirty-four- to 7-day-old F. candida were fed with wheat powder spiked with 0, 500, and 1500 μg Pb g-1 for four weeks and were then offered to 32-35 day-old H. aculeifer as prey for two weeks. Lead concentrations in tissues of both the collembolan and its predator increased with increasing total Pb in wheat. The Pb bioaccumulation factor (BAF) between predatory mites and collembolans was 1.05-1.57 and was significantly higher than that from wheat to collembolan. Diverse microbial communities were observed in both the collembolan and predator guts, consisting of (at phylum level) Proteobacteria (~77%), Bacteroidetes (~12%), Firmicutes (~4%) and Actinobacteria (~2%) in the collembolan gut and Proteobacteria (~93%) accounted for the most of the microbes in the gut of the predatory mite. The 15N fraction in the collembolan and the predatory mite was negatively correlated with the gene sequence number of COG (clusters of orthologous groups of proteins) functional categories in energy production and conversion (collembolan -0.693, mite 0.683), amino acid transport and metabolism (collembolan -0.194, mite 0.696) and defence mechanisms (collembolan -0.688, mite 0.688*). The 15N fraction in collembolan and predatory mite tissues increased significantly initially and then decreased with increasing Pb in wheat, perhaps due to the significant shift in the gut microbiome of those animals fed with Pb-contaminated food and their food intake. The key microbe (Xanthobacteraceae) that contributed to nitrogen cycling and organic matter decomposition decreased significantly in the guts of both collembolans and mites. The 15N and gut microbes in soil animals have considerable potential as biomarkers of food Pb contamination in soil food webs.

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