Carrageenan oligosaccharides and associated carrageenan-degrading bacteria induce intestinal inflammation in germ-free mice

Yeshi Yin; Miaomiao Li; Weizhong Gu; Benhua Zeng; Wei Liu; Liying Zhu; Xionge Pi; Donald A. Primerano; Hongwei D. Yu; Hong Wei; Guangli Yu; Xin Wang

doi:10.1016/j.jgg.2021.08.001

Volume 48 Issue 9

Sep. 2021

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Article Navigation > Journal of Genetics and Genomics > 2021 > 48(9): 815-824

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Carrageenan oligosaccharides and associated carrageenan-degrading bacteria induce intestinal inflammation in germ-free mice

doi: 10.1016/j.jgg.2021.08.001

a. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Food Research, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China;
b. Shandong Provincial Key Laboratory of Glycoscience and Glycotechnology, Key Laboratory of Marine Drugs of Ministry of Education, Ocean University of China, Qingdao 266100, China;
c. Department of Gastroenterology, Children's Hospital, Zhejiang University School of Medicine, Hangzhou 310057, China;
d. Department of Laboratory Animal Science, College of Basic Medical Sciences, Third Military Medical University, Chongqing 400038, China;
e. Department of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25701, United States

Funds:

Xin Wang was supported by National Natural Science Foundation of China (NSFC, 31870106), Key Research & Development of Zhejiang Province (2018C02048), and State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agroproducts (2010DS0024-ZZ006). Guangli Yu was supported by National Natural Science Foundation of China (NSFC, 81991522), the National Science and Technology Major Project for Significant New Drug Development (2018ZX09735004), and Taishan Scholar Climbing Project (TSPD20210304). Yeshi Yin was supported by Distinguished Young Scholars of Hunan Natural Science Foundation (2020JJ2016). HDY was supported by NIGMS R44GM113545 and P20GM103434. DAP is supported by NIGMS WV-INBRE P20GM103434.

Received Date: 2021-08-05
Accepted Date: 2021-08-07
Publish Date: 2021-08-13

Abstract

Abstract

Carrageenans (CGNs) are widely used in foods and pharmaceuticals although their safety remains controversial. To investigate the effects of CGNs and CGN-degrading bacteria in the human colon, we screened for CGN degradation by human fecal microbiota, and for inflammatory response to CGNs and/or CGN-degrading bacteria in germ free mice. Thin-layer chromatography indicated that high molecular weight (MW) CGNs (≥ 100 kDa) remained undegraded in the presence of human fecal microbiota, whereas low MW CGNs, i.e., κ-carrageenan oligosaccharides (KCO,~4.5 kDa) were degraded when exposed to seven of eight human fecal samples, although sulfate groups were not removed during degradation. Bacteroides xylanisolvens and Escherichia coli isolates from fecal samples apparently degraded KCO synergistically, with B. xylanisolvens serving as the primary degrader. Combined treatment of KCO with KCO-degrading bacteria led to greater pro-inflammatory effects in the colon and rectum of germ-free mice than either KCO or bacteria alone. Similarly, p-p38-, CD3-, and CD79a-positive immune cells were more abundant in combined treatment group mice than in either single treatment group. Our study shows that KCO-degrading bacteria and the low MW products of KCO can promote proinflammatory effects in mice, and represent two key markers for evaluating CGN safety in foods or medicines.
- Carrageenans,
- Carrageenan oligosaccharides,
- Oligosaccharide degrading bacteria,
- Intestinal inflammatory,
- Germ-free mouse

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References(29)

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