Lactobacillus fermentum HNU312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposure

Lead exposure is a global public health safety issue that severely disrupts brain development and causes damage to the nervous system in early life. Probiotics and gut microbes have been highlighted for their critical roles in mitigating lead toxicity. However, the underlying mechanisms by which the...

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Main Authors: Zeng Zhang, Jiahe Li, Shuaiming Jiang, Meng Xu, Teng Ma, Zhihong Sun, Jiachao Zhang
Format: Article
Language:English
Published: Elsevier 2023-02-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651323000477
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author Zeng Zhang
Jiahe Li
Shuaiming Jiang
Meng Xu
Teng Ma
Zhihong Sun
Jiachao Zhang
author_facet Zeng Zhang
Jiahe Li
Shuaiming Jiang
Meng Xu
Teng Ma
Zhihong Sun
Jiachao Zhang
author_sort Zeng Zhang
collection DOAJ
description Lead exposure is a global public health safety issue that severely disrupts brain development and causes damage to the nervous system in early life. Probiotics and gut microbes have been highlighted for their critical roles in mitigating lead toxicity. However, the underlying mechanisms by which they work yet to be fully explored. Here, we designed a two-stage experiment using the probiotic Lactobacillus fermentum HNU312 (Lf312) to uncover how probiotics alleviate lead toxicity to the brain during early life. First, we explored the tolerance and adsorption of Lf312 to lead in vitro. Second, the adsorption capacity of the strain was determined and confirmed in vivo. The shotgun metagenome sequencing showed lead exposure-induced imbalance and dysfunction of the gut microbiome. In contrast, Lf312 intake significantly modulated the structure of the microbiome, increased the abundance of beneficial bacteria and short-chain fatty acids (SCFAs)-producing bacteria, and upregulated function-related metabolic pathways such as antioxidants. Notably, Lf312 enhanced the integrity of the blood-brain barrier by increasing the levels of SCFAs in the gut, alleviated inflammation in the brain, and ultimately improved anxiety-like and depression-like behaviours induced by lead exposure in mice. Subsequently, the effective mechanism was confirmed, highlighting that Lf312 worked through integrated strategies, including ionic adsorption and microbiota-gut-brain axis regulation. Collectively, this work elucidated the mechanism by which the gut microbiota mitigates the toxic effects of lead in the brain and provides preventive measures and intervention measures for brain damage due to mass lead poisoning in children.
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spelling doaj.art-e98d7cf1e8784f1283ec1fd6ddfd37c02023-02-02T04:47:03ZengElsevierEcotoxicology and Environmental Safety0147-65132023-02-01251114543Lactobacillus fermentum HNU312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposureZeng Zhang0Jiahe Li1Shuaiming Jiang2Meng Xu3Teng Ma4Zhihong Sun5Jiachao Zhang6College of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou 570228, Hainan, ChinaCollege of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou 570228, Hainan, ChinaCollege of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou 570228, Hainan, ChinaCollege of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou 570228, Hainan, ChinaKey Laboratory of Dairy Biotechnology and Engineering, Ministry of Education P. R. C., Key Laboratory of Dairy Products Processing, Ministry of Agriculture and Rural Affairs China, Inner Mongolia Agricultural University, Hohhot 010018, ChinaKey Laboratory of Dairy Biotechnology and Engineering, Ministry of Education P. R. C., Key Laboratory of Dairy Products Processing, Ministry of Agriculture and Rural Affairs China, Inner Mongolia Agricultural University, Hohhot 010018, China; Corresponding author.College of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou 570228, Hainan, China; One Health Institute, Hainan University, Haikou, Hainan 570228, China; Corresponding author at: College of Food Science and Engineering, Key Laboratory of Food Nutrition and Functional Food of Hainan Province, Hainan University, Haikou 570228, Hainan, China.Lead exposure is a global public health safety issue that severely disrupts brain development and causes damage to the nervous system in early life. Probiotics and gut microbes have been highlighted for their critical roles in mitigating lead toxicity. However, the underlying mechanisms by which they work yet to be fully explored. Here, we designed a two-stage experiment using the probiotic Lactobacillus fermentum HNU312 (Lf312) to uncover how probiotics alleviate lead toxicity to the brain during early life. First, we explored the tolerance and adsorption of Lf312 to lead in vitro. Second, the adsorption capacity of the strain was determined and confirmed in vivo. The shotgun metagenome sequencing showed lead exposure-induced imbalance and dysfunction of the gut microbiome. In contrast, Lf312 intake significantly modulated the structure of the microbiome, increased the abundance of beneficial bacteria and short-chain fatty acids (SCFAs)-producing bacteria, and upregulated function-related metabolic pathways such as antioxidants. Notably, Lf312 enhanced the integrity of the blood-brain barrier by increasing the levels of SCFAs in the gut, alleviated inflammation in the brain, and ultimately improved anxiety-like and depression-like behaviours induced by lead exposure in mice. Subsequently, the effective mechanism was confirmed, highlighting that Lf312 worked through integrated strategies, including ionic adsorption and microbiota-gut-brain axis regulation. Collectively, this work elucidated the mechanism by which the gut microbiota mitigates the toxic effects of lead in the brain and provides preventive measures and intervention measures for brain damage due to mass lead poisoning in children.http://www.sciencedirect.com/science/article/pii/S0147651323000477Lactobacillus fermentumChronic lead exposureIntracerebral inflammationOxidative damageGut microbiomeShort-chain fatty acids
spellingShingle Zeng Zhang
Jiahe Li
Shuaiming Jiang
Meng Xu
Teng Ma
Zhihong Sun
Jiachao Zhang
Lactobacillus fermentum HNU312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposure
Ecotoxicology and Environmental Safety
Lactobacillus fermentum
Chronic lead exposure
Intracerebral inflammation
Oxidative damage
Gut microbiome
Short-chain fatty acids
title Lactobacillus fermentum HNU312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposure
title_full Lactobacillus fermentum HNU312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposure
title_fullStr Lactobacillus fermentum HNU312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposure
title_full_unstemmed Lactobacillus fermentum HNU312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposure
title_short Lactobacillus fermentum HNU312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposure
title_sort lactobacillus fermentum hnu312 alleviated oxidative damage and behavioural abnormalities during brain development in early life induced by chronic lead exposure
topic Lactobacillus fermentum
Chronic lead exposure
Intracerebral inflammation
Oxidative damage
Gut microbiome
Short-chain fatty acids
url http://www.sciencedirect.com/science/article/pii/S0147651323000477
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