Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics

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

doi:10.3389/fmicb.2023.1278271

Integrative analysis of microbiota and metabolomics in chromium-exposed silkworm (Bombyx mori) midguts based on 16S rDNA sequencing and LC/MS metabolomics

Front Microbiol. 2023 Oct 25:14:1278271. doi: 10.3389/fmicb.2023.1278271. eCollection 2023.

Authors

Ya-Zhen Chen^#^{1

2}, Wan-Tao Rong^#^{1

2}, Ying-Can Qin^{1

2}, Lin-Yuan Lu^{1

2}, Jing Liu^{1

2}, Ming-Jie Li^{1

2}, Lei Xin^{1

2}, Xiao-Dong Li^{1

2}, De-Long Guan^{1

2}

Affiliations

¹ Guangxi Key Laboratory of Sericulture Ecology and Applied Intelligent Technology, Hechi University, Hechi, China.
² Guangxi Collaborative Innovation Center of Modern Sericulture and Silk, Hechi University, Hechi, China.

^# Contributed equally.

Abstract

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.

Keywords: chromium exposure; gut microbiota; metabolomics; multi-omics; silkworms.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was funded by the Special Project of Guangxi Collaborative Innovation Center of Modern Sericulture and Silk (2022GXCSSC03, 2022GXCSSC04, 2022GXCSSC09), Guangxi University Young and Middle-aged Teachers’ Basic Research Ability Improvement Project 2023KY0638.