Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics
The gut microbiota, a complex ecosystem integral to host wellbeing, is modulated by environmental triggers, including exposure to heavy metals such as chromium. This study aims to comprehensively explore chromium-induced gut microbiota and metabolomic shifts in the quintessential lepidopteran model...
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Frontiers Media S.A.
2023-10-01
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Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1278271/full |
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author | Ya-Zhen Chen Ya-Zhen Chen Wan-Tao Rong Wan-Tao Rong Ying-Can Qin Ying-Can Qin Lin-Yuan Lu Lin-Yuan Lu Jing Liu Jing Liu Ming-Jie Li Ming-Jie Li Lei Xin Lei Xin Xiao-Dong Li Xiao-Dong Li De-Long Guan De-Long Guan |
author_facet | Ya-Zhen Chen Ya-Zhen Chen Wan-Tao Rong Wan-Tao Rong Ying-Can Qin Ying-Can Qin Lin-Yuan Lu Lin-Yuan Lu Jing Liu Jing Liu Ming-Jie Li Ming-Jie Li Lei Xin Lei Xin Xiao-Dong Li Xiao-Dong Li De-Long Guan De-Long Guan |
author_sort | Ya-Zhen Chen |
collection | DOAJ |
description | The gut microbiota, a complex ecosystem integral to host wellbeing, is modulated by environmental triggers, including exposure to heavy metals such as chromium. This study aims to comprehensively explore chromium-induced gut microbiota and metabolomic shifts in the quintessential lepidopteran model organism, the silkworm (Bombyx mori). The research deployed 16S rDNA sequence analysis and LC/MS metabolomics in its experimental design, encompassing a control group alongside low (12 g/kg) and high (24 g/kg) feeding chromium dosing regimens. Considerable heterogeneity in microbial diversity resulted between groups. Weissella emerged as potentially resilient to chromium stress, while elevated Propionibacterium was noted in the high chromium treatment group. Differential analysis tools LEfSe and random forest estimation identified key species like like Cupriavidus and unspecified Myxococcales, offering potential avenues for bioremediation. An examination of gut functionality revealed alterations in the KEGG pathways correlated with biosynthesis and degradation, suggesting an adaptive metabolic response to chromium-mediated stress. Further results indicated consequential fallout in the context of metabolomic alterations. These included an uptick in histidine and dihydropyrimidine levels under moderate-dose exposure and a surge of gentisic acid with high-dose chromium exposure. These are critical players in diverse biological processes ranging from energy metabolism and stress response to immune regulation and antioxidative mechanisms. Correlative analyses between bacterial abundance and metabolites mapped noteworthy relationships between marker bacterial species, such as Weissella and Pelomonas, and specific metabolites, emphasizing their roles in enzyme regulation, synaptic processes, and lipid metabolism. Probiotic bacteria showed robust correlations with metabolites implicated in stress response, lipid metabolism, and antioxidant processes. Our study reaffirms the intricate ties between gut microbiota and metabolite profiles and decodes some systemic adaptations under heavy-metal stress. It provides valuable insights into ecological and toxicological aspects of chromium exposure that can potentially influence silkworm resilience. |
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spelling | doaj.art-e174929f826a476eb9ebdb1ccff8e5032023-10-26T06:17:21ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-10-011410.3389/fmicb.2023.12782711278271Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomicsYa-Zhen Chen0Ya-Zhen Chen1Wan-Tao Rong2Wan-Tao Rong3Ying-Can Qin4Ying-Can Qin5Lin-Yuan Lu6Lin-Yuan Lu7Jing Liu8Jing Liu9Ming-Jie Li10Ming-Jie Li11Lei Xin12Lei Xin13Xiao-Dong Li14Xiao-Dong Li15De-Long Guan16De-Long Guan17Guangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaGuangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaGuangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaGuangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaGuangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaGuangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaGuangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaGuangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaGuangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, ChinaGuangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, ChinaThe gut microbiota, a complex ecosystem integral to host wellbeing, is modulated by environmental triggers, including exposure to heavy metals such as chromium. This study aims to comprehensively explore chromium-induced gut microbiota and metabolomic shifts in the quintessential lepidopteran model organism, the silkworm (Bombyx mori). The research deployed 16S rDNA sequence analysis and LC/MS metabolomics in its experimental design, encompassing a control group alongside low (12 g/kg) and high (24 g/kg) feeding chromium dosing regimens. Considerable heterogeneity in microbial diversity resulted between groups. Weissella emerged as potentially resilient to chromium stress, while elevated Propionibacterium was noted in the high chromium treatment group. Differential analysis tools LEfSe and random forest estimation identified key species like like Cupriavidus and unspecified Myxococcales, offering potential avenues for bioremediation. An examination of gut functionality revealed alterations in the KEGG pathways correlated with biosynthesis and degradation, suggesting an adaptive metabolic response to chromium-mediated stress. Further results indicated consequential fallout in the context of metabolomic alterations. These included an uptick in histidine and dihydropyrimidine levels under moderate-dose exposure and a surge of gentisic acid with high-dose chromium exposure. These are critical players in diverse biological processes ranging from energy metabolism and stress response to immune regulation and antioxidative mechanisms. Correlative analyses between bacterial abundance and metabolites mapped noteworthy relationships between marker bacterial species, such as Weissella and Pelomonas, and specific metabolites, emphasizing their roles in enzyme regulation, synaptic processes, and lipid metabolism. Probiotic bacteria showed robust correlations with metabolites implicated in stress response, lipid metabolism, and antioxidant processes. Our study reaffirms the intricate ties between gut microbiota and metabolite profiles and decodes some systemic adaptations under heavy-metal stress. It provides valuable insights into ecological and toxicological aspects of chromium exposure that can potentially influence silkworm resilience.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1278271/fullchromium exposuresilkwormsgut microbiotametabolomicsmulti-omics |
spellingShingle | Ya-Zhen Chen Ya-Zhen Chen Wan-Tao Rong Wan-Tao Rong Ying-Can Qin Ying-Can Qin Lin-Yuan Lu Lin-Yuan Lu Jing Liu Jing Liu Ming-Jie Li Ming-Jie Li Lei Xin Lei Xin Xiao-Dong Li Xiao-Dong Li De-Long Guan De-Long Guan Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics Frontiers in Microbiology chromium exposure silkworms gut microbiota metabolomics multi-omics |
title | Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics |
title_full | Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics |
title_fullStr | Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics |
title_full_unstemmed | Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics |
title_short | Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics |
title_sort | integrative analysis of microbiota and metabolomics in chromium exposed silkworm bombyx mori midguts based on 16s rdna sequencing and lc ms metabolomics |
topic | chromium exposure silkworms gut microbiota metabolomics multi-omics |
url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1278271/full |
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