A new capacity of gut microbiota: Fermentation of engineered inorganic carbon nanomaterials into endogenous organic metabolites

Author:

Cui Xuejing12ORCID,Wang Xiaoyu13,Chang Xueling4ORCID,Bao Lin13,Wu Junguang13,Tan Zhiqiang5ORCID,Chen Jinmei6,Li Jiayang1,Gao Xingfa1ORCID,Ke Pu Chun2ORCID,Chen Chunying123ORCID

Affiliation:

1. Chinese Academy of Sciences Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety and Center for Excellence in Nanoscience, National Center for Nanoscience and Technology of China, Beijing 100190, China

2. The GBA National Institute for Nanotechnology Innovation, Guangzhou 510700, Guangdong, China

3. School of Nano Science and Technology, University of Chinese Academy of Sciences, Beijing 101400, China

4. Chinese Academy of Sciences Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Institute of High Energy Physics, Beijing 100049, China

5. State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China

6. SCIEX China, Beijing 100020, China

Abstract

Carbon-based nanomaterials (CNMs) have recently been found in humans raising a great concern over their adverse roles in the hosts. However, our knowledge of the in vivo behavior and fate of CNMs, especially their biological processes elicited by the gut microbiota, remains poor. Here, we uncovered the integration of CNMs (single-walled carbon nanotubes and graphene oxide) into the endogenous carbon flow through degradation and fermentation, mediated by the gut microbiota of mice using isotope tracing and gene sequencing. As a newly available carbon source for the gut microbiota, microbial fermentation leads to the incorporation of inorganic carbon from the CNMs into organic butyrate through the pyruvate pathway. Furthermore, the butyrate-producing bacteria are identified to show a preference for the CNMs as their favorable source, and excessive butyrate derived from microbial CNMs fermentation further impacts on the function (proliferation and differentiation) of intestinal stem cells in mouse and intestinal organoid models. Collectively, our results unlock the unknown fermentation processes of CNMs in the gut of hosts and underscore an urgent need for assessing the transformation of CNMs and their health risk via the gut-centric physiological and anatomical pathways.

Funder

MOST | National Key Research and Development Program of China

MOST | National Natural Science Foundation of China

Major Instrument project of National Natural Science Foundation of China

Innovative Research Group Project of the National Natural Science Foundation of China

CAS international cooperative project

CAS Interdisciplinary Innovation Team, The CAS Key Research Program for Frontier Sciences

Research and Development Project in Key Areas of Guangdong Province

CAMS Innovation Fund for Medical Sciences

Strategiic Priority Research Program of Chinese Academy of Sciences

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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