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Lactobacillus plantarum-Mediated Regulation of Dietary Aluminum Induces Changes in the Human Gut Microbiota: an In Vitro Colonic Fermentation Study

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Abstract

The gut microbiota has been identified as a target of toxic metals and a potentially crucial mediator of the bioavailability and toxicity of these metals. In this study, we show that aluminum (Al) exposure, even at low dose, affected the growth of representative strains from the human intestine via pure culture experiments. In vitro, Lactobacillus plantarum CCFM639 could bind Al on its cell surface as shown by electron microscopy and energy dispersive X-ray analysis. The potential of L. plantarum CCFM639 to reverse changes in human intestine microbiota induced by low-dose dietary Al exposure was investigated using an in vitro colonic fermentation model. Batch fermenters were inoculated with fresh stool samples from healthy adult donors and supplemented with 86 mg/L Al and/or 109 CFU of L. plantarum CCFM639. Al exposure significantly increased the relative abundances of Bacteroidetes (Prevotella), Proteobacteria (Escherichia), Actinobacteria (Collinsella), Euryarchaeota (Methanobrevibacter), and Verrucomicrobiaceae and decreased Firmicutes (Streptococcus, Roseburia, Ruminococcus, Dialister, Coprobacillus). Some changes were reversed by the inclusion of L. plantarum CCFM639. Alterations in gut microbiota induced by Al and L. plantarum CCFM639 inevitably led to changes in metabolite levels. The short-chain fatty acid (SCFAs) contents were reduced after Al exposure, but L. plantarum CCFM639 could elevate their levels. SCFAs had positive correlations with beneficial bacteria, such as Dialister, Streptococcus, Roseburia, and negative correlations with Erwinia, Escherichia, and Serratia. Therefore, dietary Al exposure altered the composition and structure of the human gut microbiota, and this was partially mitigated by L. plantarum CCFM639. This probiotic supplementation is potentially a promising and safe approach to alleviate the harmful effects of dietary Al exposure.

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Acknowledgments

We thank Kathryn Cross for electron microscopy analysis. We also thank Bhavika A. Parmanand who helped in the colonic fermentation study.

Funding

This work was supported by the Natural Science Foundation of Jiangsu Province (BK20180603), National Natural Science Foundation of China Key Program (31772090, 31820103010, 31530056), the Postdoctoral Science Foundation of China (2018M642166), the General Financial Grant from the Jiangsu Postdoctoral Science Foundation (2018K016A), the Self-determined Research Program of Jiangnan University (JUSRP11847), BBSRC Newton Fund Joint Centre Award, the National First-Class Discipline Program of Food Science and Technology (JUFSTR20180102), Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province, and BBSRC Institute Strategic Program Grant (BB/R012490/1, BBS/E/F/000PR10356).

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  1. Leilei Yu and Hui Duan contributed equally to this study.

Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, China

    Leilei Yu, Shi Cen, Fengwei Tian, Jianxin Zhao, Hao Zhang, Qixiao Zhai & Wei Chen

  2. School of Food Science and Technology, Jiangnan University, Wuxi, 214122, China

    Leilei Yu, Hui Duan, Shi Cen, Fengwei Tian, Jianxin Zhao, Hao Zhang, Qixiao Zhai & Wei Chen

  3. International Joint Research Laboratory for Probiotics at Jiangnan University, Wuxi, 214122, China

    Leilei Yu, Fengwei Tian, Qixiao Zhai & Arjan Narbad

  4. Gut Health and Microbiome Institute Strategic Programme, Quadram Institute Bioscience, Norwich, NR4 7UQ, UK

    Lee Kellingray, Melinda J Mayer & Arjan Narbad

  5. National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, 214122, China

    Jianxin Zhao, Hao Zhang & Wei Chen

  6. (Yangzhou) Institute of Food Biotechnology, Jiangnan University, Yangzhou, 225004, China

    Hao Zhang

  7. Department of Medicine, Faculty of Medicine and Health Sciences, University of East Anglia, Norwich, NR4 7TJ, UK

    Gwénaëlle Le Gall

  8. Beijing Innovation Centre of Food Nutrition and Human Health, Beijing Technology & Business University, Beijing, 100048, China

    Wei Chen

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Contributions

Conceptualization: Qixiao Zhai, Wei Chen, and Arjan Narbad. Data curation: Leilei Yu, Hui Duan, and Shi Cen. Funding acquisition: Fengwei Tian, Qixiao Zhai, Wei Chen, and Arjan Narbad. Investigation, Leilei Yu and Qixiao Zhai; Methodology, Leilei Yu, Melinda Mayer, and Gwénaëlle Le Gall. Project administration: Lee Kellingray, Melinda Mayer, and Arjan Narbad. Supervision, Fengwei Tian, Jianxin Zhao, and Hao Zhang. Writing: original draft, Leilei Yu, and Hui Duan. Writing–review and editing: Leilei Yu, Hui Duan, Melinda Mayer, and Arjan Narbad.

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Correspondence to Qixiao Zhai.

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Yu, L., Duan, H., Kellingray, L. et al. Lactobacillus plantarum-Mediated Regulation of Dietary Aluminum Induces Changes in the Human Gut Microbiota: an In Vitro Colonic Fermentation Study. Probiotics & Antimicro. Prot. 13, 398–412 (2021). https://doi.org/10.1007/s12602-020-09677-0

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