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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Main Authors: Ya-Zhen Chen, Wan-Tao Rong, Ying-Can Qin, Lin-Yuan Lu, Jing Liu, Ming-Jie Li, Lei Xin, Xiao-Dong Li, De-Long Guan
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Microbiology
Subjects:
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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