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为什么中华大蟾蜍蝌蚪在铅污染环境中长得更大?肠道微生物群起了作用。

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

作者信息

Lv Yan, Chang Liming, Liu Jiongyu, Chen Qiheng, Jiang Jianping, Zhu Wei

机构信息

Chengdu Institute of Biology, Chinese Academy of Science, Chengdu 610041, China.

Chengdu Institute of Biology, Chinese Academy of Science, Chengdu 610041, China.

出版信息

Ecotoxicol Environ Saf. 2023 Nov 15;267:115601. doi: 10.1016/j.ecoenv.2023.115601. Epub 2023 Oct 25.

DOI:10.1016/j.ecoenv.2023.115601
PMID:37890260
Abstract

The impacts of lead/Pb 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 Pb or by the multiple toxic mechanisms/pathways of Pb. To examine these hypotheses, we tested how Bufo gargarizans tadpoles responded to Pb(NO) (100 and 200 μg/L Pb) using transcriptomics and microbiomics, with NaNO and blank groups as controls. Tadpoles exposed to Pb(NO) showed delayed development while increased somatic growth in a dose-dependent manner, which can be attributed to the effects of NO and Pb, respectively. Tadpole transcriptomics revealed that exposure to NO downregulated the MAPK pathway at transcriptional level, explaining the development-suppressing effect of NO; while Pb 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 Pb-exposed tadpoles. Pb 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 Pb 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 Pb-exposed tadpoles. In summary, our results suggest multiple toxic pathways of Pb, and the gut microbiota may affect the pollution outcomes on animals.

摘要

铅(Pb)对生态系统的影响已受到广泛关注。生长抑制是铅化合物对水生动物的主要毒性作用,然而,一些研究也报道了它们的促生长作用。这些复杂的结果可能由与铅相伴的阴离子或铅的多种毒性机制/途径来解释。为了验证这些假设,我们以硝酸钠组和空白组作为对照,利用转录组学和微生物组学方法,测试了中华大蟾蜍蝌蚪对硝酸铅(100和200μg/L铅)的反应。暴露于硝酸铅的蝌蚪发育延迟,而躯体生长呈剂量依赖性增加,这可分别归因于硝酸根和铅的作用。蝌蚪转录组学显示,暴露于硝酸根会在转录水平下调丝裂原活化蛋白激酶(MAPK)途径,这解释了硝酸根的发育抑制作用;而铅会上调解毒途径(如细胞色素P450介导的外源性物质代谢和谷胱甘肽代谢)的转录,这表明细胞应激,因此与暴露于铅的蝌蚪的生长优势相矛盾。铅暴露极大地改变了蝌蚪的肠道微生物群,根据微生物功能分析,其特征是多糖和碳水化合物利用增加,而脂肪酸和氨基酸消耗减少。在来自不同铅污染环境的野外采集蝌蚪中也观察到了类似的肠道微生物变化。肠道微生物群的这种代谢转变可能提高了整体食物利用效率,并增加了脂肪酸和氨基酸向宿主的分配,这解释了暴露于铅的蝌蚪的生长优势。总之,我们的结果表明铅存在多种毒性途径,并且肠道微生物群可能会影响动物对污染的反应结果。

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