Effects of long-term metal exposure on the structure and co-occurrence patterns of the oral microbiota of residents around a mining area

Shuwei Pei; Lu Feng; Yonghua Zhang; Jiangyun Liu; Jia Li; Qiwen Zheng; Xingrong Liu; Bin Luo; Ye Ruan; Huan Li; Weigang Hu; Jingping Niu; Tian Tian

doi:10.3389/fmicb.2023.1264619

Effects of long-term metal exposure on the structure and co-occurrence patterns of the oral microbiota of residents around a mining area

Front Microbiol. 2023 Oct 19:14:1264619. doi: 10.3389/fmicb.2023.1264619. eCollection 2023.

Authors

Shuwei Pei¹, Lu Feng², Yonghua Zhang³, Jiangyun Liu¹, Jia Li¹, Qiwen Zheng¹, Xingrong Liu¹, Bin Luo¹, Ye Ruan¹, Huan Li¹, Weigang Hu⁴, Jingping Niu¹, Tian Tian¹

Affiliations

¹ School of Public Health, Lanzhou University, Lanzhou, Gansu, China.
² School of Stomatology, Lanzhou University, Lanzhou, Gansu, China.
³ Child Health Department, Lanzhou Maternal and Child Health Care Hospital, Lanzhou, Gansu, China.
⁴ State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystems, College of Ecology, Lanzhou University, Lanzhou, China.

Abstract

Objectives: The aim of our study was to investigate the impact of long-term exposure to heavy metals on the microbiome of the buccal mucosa, to unveil the link between environmental contamination and the oral microbial ecosystem, and to comprehend its potential health implications.

Methods: Subjects were divided into two groups: the exposure group and the control group. We collected samples of buccal mucosa, soil, and blood, and conducted microbial diversity analysis on both groups of oral samples using 16S rRNA gene sequencing. The concentrations of heavy metals in blood and soil samples were also determined. Additionally, microbial networks were constructed for the purpose of topological analysis.

Results: Due to long-term exposure to heavy metals, the relative abundance of Rhodococcus, Delftia, Fusobacterium, and Peptostreptococcus increased, while the abundance of Streptococcus, Gemella, Prevotella, Granulicatella, and Porphyromonas decreased. The concentrations of heavy metals in the blood (Pb, Cd, Hg, and Mo) were associated with the growth of Rhodococcus, Delftia, Porphyromonas, and Gemella. In addition, the relative abundances of some pathogenic bacteria, such as Streptococcus anginosus, S. gordonii, and S. mutans, were found to be enriched in the exposure group. Compared to the exposure group network, the control group network had a greater number of nodes, modules, interactive species, and keystone taxa. Module hubs and connectors in the control group converted into peripherals in the exposure group, indicating that keystone taxa changed. Metals in the blood (Pb, Cd, Hg, and Mo) were drivers of the microbial network of the buccal mucosa, which can have adverse effects on the network, thus providing conditions for the occurrence of certain diseases.

Conclusion: Long-term exposure to multiple metals perturbs normal bacterial communities in the buccal mucosa of residents in contaminated areas. This exposure reduces the complexity and stability of the microbial network and increases the risk of developing various diseases.

Keywords: 16S rRNA gene sequencing; bacteria; buccal mucosa; heavy metal; keystone taxa; network analysis.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. We are grateful for financial support from the National Natural Science Foundation of China (nos. 32001125 and 81872578), the Fundamental Research Funds for the Central Universities (lzujbky-2021-24), and the Science and Technology Program of Lanzhou, China (no. 2022-2-108).