Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in China

Undernutrition (UN) is a worldwide concern affecting morbidity and mortality among children, but the safety and long-term efficacy of its current treatments remain controversial. Recent evidence showing the roles of the gut microbiome (GM) in nutrient absorption indicates its usefulness in alternati...

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Main Authors: Dongfang Li, Yinhu Li, Wenkui Dai, Huihui Wang, Chuangzhao Qiu, Su Feng, Qian Zhou, Wenjian Wang, Xin Feng, Kaihu Yao, Yanhong Liu, Yonghong Yang, Zhenyu Yang, Ximing Xu, Shuaicheng Li, Jurong Wei, Ke Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02635/full
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author Dongfang Li
Dongfang Li
Yinhu Li
Wenkui Dai
Huihui Wang
Chuangzhao Qiu
Su Feng
Qian Zhou
Wenjian Wang
Xin Feng
Kaihu Yao
Yanhong Liu
Yonghong Yang
Yonghong Yang
Yonghong Yang
Zhenyu Yang
Ximing Xu
Shuaicheng Li
Jurong Wei
Ke Zhou
spellingShingle Dongfang Li
Dongfang Li
Yinhu Li
Wenkui Dai
Huihui Wang
Chuangzhao Qiu
Su Feng
Qian Zhou
Wenjian Wang
Xin Feng
Kaihu Yao
Yanhong Liu
Yonghong Yang
Yonghong Yang
Yonghong Yang
Zhenyu Yang
Ximing Xu
Shuaicheng Li
Jurong Wei
Ke Zhou
Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in China
Frontiers in Microbiology
childhood undernutrition
gut microbiome markers
Bacteroides
iron transporter
nutritional indicators
author_facet Dongfang Li
Dongfang Li
Yinhu Li
Wenkui Dai
Huihui Wang
Chuangzhao Qiu
Su Feng
Qian Zhou
Wenjian Wang
Xin Feng
Kaihu Yao
Yanhong Liu
Yonghong Yang
Yonghong Yang
Yonghong Yang
Zhenyu Yang
Ximing Xu
Shuaicheng Li
Jurong Wei
Ke Zhou
author_sort Dongfang Li
title Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in China
title_short Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in China
title_full Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in China
title_fullStr Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in China
title_full_unstemmed Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in China
title_sort intestinal bacteroides sp. imbalance associated with the occurrence of childhood undernutrition in china
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-11-01
description Undernutrition (UN) is a worldwide concern affecting morbidity and mortality among children, but the safety and long-term efficacy of its current treatments remain controversial. Recent evidence showing the roles of the gut microbiome (GM) in nutrient absorption indicates its usefulness in alternative interventions to treat UN safely with sustainable amelioration. To enhance our understanding of the GM and childhood undernutrition, we deep sequenced the gut metagenomes of 65 children with moderate or severe undernutrition (UN group) and 61 healthy children (HC group) to identify associated taxa and genes using a two-stage validation scheme. At stage I, 54 UN patients and 51 healthy children were enrolled for the discovery of GM markers in UN children. The accuracy of the markers was then tested in an additional 11 UN patients and 10 healthy children at stage II. Compared to the HC group, the UN group had lower richness in microbial genes (P = 0.005, FDR = 0.005) and species (P = 0.002, FDR = 0.002). The distributions of bacterial genes enable the identification of 16 gene markers with which to discriminate UN patients with high accuracy [averaged areas under the receiver operating curve (AUC) = 0.87], including three Bacteroides uniformis genes that are responsible for the synthesis of iron transporters. We also identified four species markers that enable the UN patients to be confidently discriminated from the HC children (averaged AUC = 0.91), namely Bacteroides ovatus, Bacteroides uniformis, Bacteroides uniformis, and Bacteroides vulgatus. In addition, metabolic comparison showed significantly decreased isobutyric acid (P = 0.005, FDR = 0.017) and increased isovaleric acid (P = 0.006, FDR = 0.017) in UN patients. We also identified notable correlations between microbial species and short-chain fatty acids (SCFAs) and several nutritional indicators, including acetic acid and iron (r = 0.436, P = 0.029), butyric acid and iron (r = 0.422, P = 0.036), butyric acid and lymphocyte (r = −0.309, P = 0.011), and acetic acid and total protein (r = −0.303, P = 0.043). Taken together, the distinct features of gut microbiota in UN patients highlight the taxonomic and functional shift during the development of UN and provide a solid theoretical basis for intervention in childhood undernutrition through gut microbes.
topic childhood undernutrition
gut microbiome markers
Bacteroides
iron transporter
nutritional indicators
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02635/full
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spelling doaj-290a0f91dd0c4a8f985b6b2f5e22cd922020-11-25T01:23:07ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-11-011010.3389/fmicb.2019.02635490797Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in ChinaDongfang Li0Dongfang Li1Yinhu Li2Wenkui Dai3Huihui Wang4Chuangzhao Qiu5Su Feng6Qian Zhou7Wenjian Wang8Xin Feng9Kaihu Yao10Yanhong Liu11Yonghong Yang12Yonghong Yang13Yonghong Yang14Zhenyu Yang15Ximing Xu16Shuaicheng Li17Jurong Wei18Ke Zhou19Wuhan National Laboratory for Optoelectronics, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Microbial Research, WeHealthGene Institute, Shenzhen, ChinaDepartment of Computer Science, College of Science and Engineering, City University of Hong Kong, Kowloon Tong, Hong KongDepartment of Microbial Research, WeHealthGene Institute, Shenzhen, ChinaDepartment of Clinical Nutrition, Shenzhen Children’s Hospital, Shenzhen, ChinaDepartment of Microbial Research, WeHealthGene Institute, Shenzhen, ChinaInstitute of Statistics, Nankai University, Tianjin, ChinaDepartment of Computer Science, College of Science and Engineering, City University of Hong Kong, Kowloon Tong, Hong KongDepartment of Respiratory Diseases, Shenzhen Children’s Hospital, Shenzhen, ChinaDepartment of Microbial Research, WeHealthGene Institute, Shenzhen, ChinaDepartment of Respiratory Diseases, Beijing Children’s Hospital, Beijing, ChinaDepartment of Microbial Research, WeHealthGene Institute, Shenzhen, ChinaDepartment of Microbial Research, WeHealthGene Institute, Shenzhen, ChinaDepartment of Respiratory Diseases, Shenzhen Children’s Hospital, Shenzhen, ChinaDepartment of Respiratory Diseases, Beijing Children’s Hospital, Beijing, ChinaDepartment of Microbial Research, WeHealthGene Institute, Shenzhen, ChinaInstitute of Statistics, Nankai University, Tianjin, ChinaDepartment of Computer Science, College of Science and Engineering, City University of Hong Kong, Kowloon Tong, Hong KongDepartment of Clinical Nutrition, Shenzhen Children’s Hospital, Shenzhen, ChinaWuhan National Laboratory for Optoelectronics, Huazhong University of Science and Technology, Wuhan, ChinaUndernutrition (UN) is a worldwide concern affecting morbidity and mortality among children, but the safety and long-term efficacy of its current treatments remain controversial. Recent evidence showing the roles of the gut microbiome (GM) in nutrient absorption indicates its usefulness in alternative interventions to treat UN safely with sustainable amelioration. To enhance our understanding of the GM and childhood undernutrition, we deep sequenced the gut metagenomes of 65 children with moderate or severe undernutrition (UN group) and 61 healthy children (HC group) to identify associated taxa and genes using a two-stage validation scheme. At stage I, 54 UN patients and 51 healthy children were enrolled for the discovery of GM markers in UN children. The accuracy of the markers was then tested in an additional 11 UN patients and 10 healthy children at stage II. Compared to the HC group, the UN group had lower richness in microbial genes (P = 0.005, FDR = 0.005) and species (P = 0.002, FDR = 0.002). The distributions of bacterial genes enable the identification of 16 gene markers with which to discriminate UN patients with high accuracy [averaged areas under the receiver operating curve (AUC) = 0.87], including three Bacteroides uniformis genes that are responsible for the synthesis of iron transporters. We also identified four species markers that enable the UN patients to be confidently discriminated from the HC children (averaged AUC = 0.91), namely Bacteroides ovatus, Bacteroides uniformis, Bacteroides uniformis, and Bacteroides vulgatus. In addition, metabolic comparison showed significantly decreased isobutyric acid (P = 0.005, FDR = 0.017) and increased isovaleric acid (P = 0.006, FDR = 0.017) in UN patients. We also identified notable correlations between microbial species and short-chain fatty acids (SCFAs) and several nutritional indicators, including acetic acid and iron (r = 0.436, P = 0.029), butyric acid and iron (r = 0.422, P = 0.036), butyric acid and lymphocyte (r = −0.309, P = 0.011), and acetic acid and total protein (r = −0.303, P = 0.043). Taken together, the distinct features of gut microbiota in UN patients highlight the taxonomic and functional shift during the development of UN and provide a solid theoretical basis for intervention in childhood undernutrition through gut microbes.https://www.frontiersin.org/article/10.3389/fmicb.2019.02635/fullchildhood undernutritiongut microbiome markersBacteroidesiron transporternutritional indicators