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Dynamic alterations of locomotor activity and the microbiota in zebrafish larvae with low concentrations of lead exposure

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Abstract

Lead (Pb) is a ubiquitous heavy metal associated with developmental and behavioral disorders. The establishment of pioneer microbiota overlaps with the development of the brain during early life, and Pb-induced developmental neurotoxicity may be partially caused by early-life microbiota dysbiosis. This study investigated the locomotor activity and the microbiota in developing zebrafish at multiple developmental time points (five days post fertilization [5 dpf], 6 dpf, and 7 dpf) under exposure to low concentrations of lead (0.05 mg/L). Time-dependent reductions in the number of activities and the average movement distance of larvae compared to the control were observed following Pb exposure. Furthermore, Pb exposure significantly altered the composition of the gut microbiota of zebrafish larvae. At the phylum level, the abundance of Proteobacteria decreased from 5 to 7 dpf, while that of Actinobacteria increased in the control groups. At the class level, the proportion of Alphaproteobacteria decreased, while that of Actinobacteria increased in the control groups. Notably, all showed the opposite trend in Pb groups. A correlation analysis between indices of locomotor activity and microbial communities revealed genus-level features that were clearly linked to the neurobehavioral performance of zebrafish. Seven genera were significantly correlated with the two performance indicators of the locomotion analysis, namely Rhodococcus, Deinococcus, Bacillus, Bosea, Bradyrhizobium, Staphylococcus, and Rhizobium. Rhizobium was dominant in zebrafish and increased in the Pb groups in a time-dependent manner. In addition, the expression levels of bdnf, trkb1, trkb2, and p75ntr changed in zebrafish from 5 to 7 dpf under Pb exposure. Collectively, these results suggest that Pb-induced neurotoxicity could potentially be treated by targeting the gut microbiota.

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Funding

This work was supported by grants from the National Natural Science Foundation of China (no. 81973071, 81773473 to XM) and Medical Science and Technology Research Foundation of Guangdong Province, China (no. A2021195 to YX).

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Authors and Affiliations

  1. School of Public Health, Guangdong Pharmaceutical University, Jianghaidadao, Guangzhou, 283, Guangdong, China

    Yuan Xia, Ziyi Li, Chunyu Wang, Junyi Li, Jian Yang, Qingsong Chen & Junyi Wang

  2. Department of Occupational Health and Occupational Medicine, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou, Guangdong, China

    Xiaoshun Zhang, Qin Zhou & Xiaojing Meng

Authors
  1. Yuan Xia
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  2. Ziyi Li
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Contributions

Yuan Xia: methodology and writing—original draft and editing. Ziyi Li.: methodology. Chunyu Wang: methodology. Xiaoshun Zhang: methodology. Junyi Li: writing—original draft. Qin Zhou: methodology. Jian Yang: methodology and writing—original draft. Qingsong Chen: conceptualization and supervision. Xiaojing Meng: conceptualization and supervision. Junyi Wang: conceptualization, supervision, and writing—review and editing. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Junyi Wang.

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All zebrafish work was approved by the Ethical Review Committee of Southern Medical University, China.

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Synopsis: BDNF signaling was identified as the link between the microbiota and behavior under Pb exposure. The bacteria Rhizobium could be a biomarker for Pb exposure and neurotoxicity.

Highlights

• Pb exposure induced alterations of locomotor activities and microbiota in zebrafish.

• BDNF signaling was the link between the microbiota and behavior with Pb exposure.

• Rhizobium could be a biomarker for Pb exposure and neurotoxicity.

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Xia, Y., Li, Z., Wang, C. et al. Dynamic alterations of locomotor activity and the microbiota in zebrafish larvae with low concentrations of lead exposure. Environ Sci Pollut Res 31, 2042–2052 (2024). https://doi.org/10.1007/s11356-023-31279-w

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