Isolation of Alginate-Degrading Bacteria from the Human Gut Microbiota and Discovery of <i>Bacteroides xylanisolvens</i> AY11-1 as a Novel Anti-Colitis Probiotic Bacterium

Alginate has been documented to prevent the development and progression of ulcerative colitis by modulating the gut microbiota. However, the bacterium that may mediate the anti-colitis effect of alginate has not been fully characterized. We hypothesized that alginate-degrading bacteria might play a...

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Main Authors: Tianyu Fu, Yamin Wang, Mingfeng Ma, Wei Dai, Lin Pan, Qingsen Shang, Guangli Yu
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Nutrients
Subjects:
Online Access:https://www.mdpi.com/2072-6643/15/6/1352
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author Tianyu Fu
Yamin Wang
Mingfeng Ma
Wei Dai
Lin Pan
Qingsen Shang
Guangli Yu
author_facet Tianyu Fu
Yamin Wang
Mingfeng Ma
Wei Dai
Lin Pan
Qingsen Shang
Guangli Yu
author_sort Tianyu Fu
collection DOAJ
description Alginate has been documented to prevent the development and progression of ulcerative colitis by modulating the gut microbiota. However, the bacterium that may mediate the anti-colitis effect of alginate has not been fully characterized. We hypothesized that alginate-degrading bacteria might play a role here since these bacteria could utilize alginate as a carbon source. To test this hypothesis, we isolated 296 strains of alginate-degrading bacteria from the human gut. <i>Bacteroides xylanisolvens</i> AY11-1 was observed to have the best capability for alginate degradation. The degradation and fermentation of alginate by <i>B. xylanisolvens</i> AY11-1 produced significant amounts of oligosaccharides and short-chain fatty acids. Further studies indicated that <i>B. xylanisolvens</i> AY11-1 could alleviate body weight loss and contraction of colon length, reduce the incidences of bleeding and attenuate mucosal damage in dextran sulfate sodium (DSS)-fed mice. Mechanistically, <i>B. xylanisolvens</i> AY11-1 improved gut dysbiosis and promoted the growth of probiotic bacteria, including <i>Blautia</i> spp. And <i>Prevotellaceae UCG-001</i>, in diseased mice. Additionally, <i>B. xylanisolvens</i> AY11-1 showed no oral toxicity and was well-tolerated in male and female mice. Altogether, we illustrate for the first time an anti-colitis effect of the alginate-degrading bacterium <i>B. xylanisolvens</i> AY11-1. Our study paves the way for the development of <i>B. xylanisolvens</i> AY11-1 as a next-generation probiotic bacterium.
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spelling doaj.art-2b9ebc741956453293e0a2bd26b999ce2023-11-17T13:04:34ZengMDPI AGNutrients2072-66432023-03-01156135210.3390/nu15061352Isolation of Alginate-Degrading Bacteria from the Human Gut Microbiota and Discovery of <i>Bacteroides xylanisolvens</i> AY11-1 as a Novel Anti-Colitis Probiotic BacteriumTianyu Fu0Yamin Wang1Mingfeng Ma2Wei Dai3Lin Pan4Qingsen Shang5Guangli Yu6Key Laboratory of Marine Drugs of Ministry of Education, Shandong Key Laboratory of Glycoscience and Glycotechnology, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Marine Drugs of Ministry of Education, Shandong Key Laboratory of Glycoscience and Glycotechnology, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Marine Drugs of Ministry of Education, Shandong Key Laboratory of Glycoscience and Glycotechnology, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Marine Drugs of Ministry of Education, Shandong Key Laboratory of Glycoscience and Glycotechnology, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Marine Drugs of Ministry of Education, Shandong Key Laboratory of Glycoscience and Glycotechnology, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Marine Drugs of Ministry of Education, Shandong Key Laboratory of Glycoscience and Glycotechnology, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, ChinaKey Laboratory of Marine Drugs of Ministry of Education, Shandong Key Laboratory of Glycoscience and Glycotechnology, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, ChinaAlginate has been documented to prevent the development and progression of ulcerative colitis by modulating the gut microbiota. However, the bacterium that may mediate the anti-colitis effect of alginate has not been fully characterized. We hypothesized that alginate-degrading bacteria might play a role here since these bacteria could utilize alginate as a carbon source. To test this hypothesis, we isolated 296 strains of alginate-degrading bacteria from the human gut. <i>Bacteroides xylanisolvens</i> AY11-1 was observed to have the best capability for alginate degradation. The degradation and fermentation of alginate by <i>B. xylanisolvens</i> AY11-1 produced significant amounts of oligosaccharides and short-chain fatty acids. Further studies indicated that <i>B. xylanisolvens</i> AY11-1 could alleviate body weight loss and contraction of colon length, reduce the incidences of bleeding and attenuate mucosal damage in dextran sulfate sodium (DSS)-fed mice. Mechanistically, <i>B. xylanisolvens</i> AY11-1 improved gut dysbiosis and promoted the growth of probiotic bacteria, including <i>Blautia</i> spp. And <i>Prevotellaceae UCG-001</i>, in diseased mice. Additionally, <i>B. xylanisolvens</i> AY11-1 showed no oral toxicity and was well-tolerated in male and female mice. Altogether, we illustrate for the first time an anti-colitis effect of the alginate-degrading bacterium <i>B. xylanisolvens</i> AY11-1. Our study paves the way for the development of <i>B. xylanisolvens</i> AY11-1 as a next-generation probiotic bacterium.https://www.mdpi.com/2072-6643/15/6/1352<i>Bacteroides xylanisolvens</i>gut microbiotaalginateulcerative colitisdextran sulfate sodiumprobiotic
spellingShingle Tianyu Fu
Yamin Wang
Mingfeng Ma
Wei Dai
Lin Pan
Qingsen Shang
Guangli Yu
Isolation of Alginate-Degrading Bacteria from the Human Gut Microbiota and Discovery of <i>Bacteroides xylanisolvens</i> AY11-1 as a Novel Anti-Colitis Probiotic Bacterium
Nutrients
<i>Bacteroides xylanisolvens</i>
gut microbiota
alginate
ulcerative colitis
dextran sulfate sodium
probiotic
title Isolation of Alginate-Degrading Bacteria from the Human Gut Microbiota and Discovery of <i>Bacteroides xylanisolvens</i> AY11-1 as a Novel Anti-Colitis Probiotic Bacterium
title_full Isolation of Alginate-Degrading Bacteria from the Human Gut Microbiota and Discovery of <i>Bacteroides xylanisolvens</i> AY11-1 as a Novel Anti-Colitis Probiotic Bacterium
title_fullStr Isolation of Alginate-Degrading Bacteria from the Human Gut Microbiota and Discovery of <i>Bacteroides xylanisolvens</i> AY11-1 as a Novel Anti-Colitis Probiotic Bacterium
title_full_unstemmed Isolation of Alginate-Degrading Bacteria from the Human Gut Microbiota and Discovery of <i>Bacteroides xylanisolvens</i> AY11-1 as a Novel Anti-Colitis Probiotic Bacterium
title_short Isolation of Alginate-Degrading Bacteria from the Human Gut Microbiota and Discovery of <i>Bacteroides xylanisolvens</i> AY11-1 as a Novel Anti-Colitis Probiotic Bacterium
title_sort isolation of alginate degrading bacteria from the human gut microbiota and discovery of i bacteroides xylanisolvens i ay11 1 as a novel anti colitis probiotic bacterium
topic <i>Bacteroides xylanisolvens</i>
gut microbiota
alginate
ulcerative colitis
dextran sulfate sodium
probiotic
url https://www.mdpi.com/2072-6643/15/6/1352
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