Gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for Helicobacter pylori

PurposeHelicobacter pylori (HP) infection is an identified risk factor for pediatric chronic gastritis (PCG), but its impact on gastric juice microbiota (GJM) remains to be further elucidated in PCG. This study aimed to analyze and compare the microbial communities and microbial interactive networks...

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Main Authors: Ying Chen, Shou-Yue Xia, Fu-Xia Ru, Jun-Jie Feng, Ji Tao, Zhi-Yuan Wei, Xiu Li, Chengjia Qian, Qiong Lin, Jian-Huan Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1112709/full
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author Ying Chen
Shou-Yue Xia
Fu-Xia Ru
Jun-Jie Feng
Ji Tao
Zhi-Yuan Wei
Xiu Li
Chengjia Qian
Qiong Lin
Jian-Huan Chen
author_facet Ying Chen
Shou-Yue Xia
Fu-Xia Ru
Jun-Jie Feng
Ji Tao
Zhi-Yuan Wei
Xiu Li
Chengjia Qian
Qiong Lin
Jian-Huan Chen
author_sort Ying Chen
collection DOAJ
description PurposeHelicobacter pylori (HP) infection is an identified risk factor for pediatric chronic gastritis (PCG), but its impact on gastric juice microbiota (GJM) remains to be further elucidated in PCG. This study aimed to analyze and compare the microbial communities and microbial interactive networks of GJM in PCG that clinically tested positive and negative for HP (HP+ and HP−, respectively).MethodsA total of 45 PCG patients aged from 6 to 16 years were recruited, including 20 HP+ and 25 HP− patients tested by culture and rapid urease test. Gastric juice samples were collected from these PCG patients and subjected to high-throughput amplicon sequencing and subsequent analysis of 16S rRNA genes.ResultsWhile no significant change in alpha diversity, significant differences in beta diversity were observed between HP+ and HP− PCG. At the genus level, Streptococcus, Helicobacter, and Granulicatella were significantly enriched in HP+ PCG, whereas Campylobacter and Absconditabacteriales (SR1) were significantly enriched in HP− PCG. Network analysis showed that Streptococcus was the only genus positively correlated with Helicobacter (r = 0.497) in the GJM network of overall PCG. Moreover, compared to HP− PCG, HP+ PCG showed a reduction in microbial network connectivity in GJM. Netshift analysis identified driver microbes including Streptococcus and other four genera, which substantially contributed to the GJM network transition from HP− PCG to HP+ PCG. Furthermore, Predicted GJM function analysis indicated up-regulated pathways related to the metabolism of nucleotides, carbohydrates, and L-Lysine, the urea cycle, as well as endotoxin peptidoglycan biosynthesis and maturation in HP+ PCG.ConclusionGJM in HP+ PCG exhibited dramatically altered beta diversity, taxonomic structure, and function, with reduced microbial network connectivity, which could be involved in the disease etiology.
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spelling doaj.art-e0b20521778a4962aace672f72146e642023-04-25T15:06:23ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11127091112709Gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for Helicobacter pyloriYing Chen0Shou-Yue Xia1Fu-Xia Ru2Jun-Jie Feng3Ji Tao4Zhi-Yuan Wei5Xiu Li6Chengjia Qian7Qiong Lin8Jian-Huan Chen9Department of Gastroenterology, Affiliated Children’s Hospital of Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, Jiangsu, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, Jiangsu, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, Jiangsu, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, Jiangsu, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, Jiangsu, ChinaLaboratory Animal Center, Jiangnan University, Wuxi, Jiangsu, ChinaDepartment of General Surgery, Affiliated Hospital of Jiangnan University, Wuxi, ChinaDepartment of Gastroenterology, Affiliated Children’s Hospital of Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, Jiangsu, ChinaPurposeHelicobacter pylori (HP) infection is an identified risk factor for pediatric chronic gastritis (PCG), but its impact on gastric juice microbiota (GJM) remains to be further elucidated in PCG. This study aimed to analyze and compare the microbial communities and microbial interactive networks of GJM in PCG that clinically tested positive and negative for HP (HP+ and HP−, respectively).MethodsA total of 45 PCG patients aged from 6 to 16 years were recruited, including 20 HP+ and 25 HP− patients tested by culture and rapid urease test. Gastric juice samples were collected from these PCG patients and subjected to high-throughput amplicon sequencing and subsequent analysis of 16S rRNA genes.ResultsWhile no significant change in alpha diversity, significant differences in beta diversity were observed between HP+ and HP− PCG. At the genus level, Streptococcus, Helicobacter, and Granulicatella were significantly enriched in HP+ PCG, whereas Campylobacter and Absconditabacteriales (SR1) were significantly enriched in HP− PCG. Network analysis showed that Streptococcus was the only genus positively correlated with Helicobacter (r = 0.497) in the GJM network of overall PCG. Moreover, compared to HP− PCG, HP+ PCG showed a reduction in microbial network connectivity in GJM. Netshift analysis identified driver microbes including Streptococcus and other four genera, which substantially contributed to the GJM network transition from HP− PCG to HP+ PCG. Furthermore, Predicted GJM function analysis indicated up-regulated pathways related to the metabolism of nucleotides, carbohydrates, and L-Lysine, the urea cycle, as well as endotoxin peptidoglycan biosynthesis and maturation in HP+ PCG.ConclusionGJM in HP+ PCG exhibited dramatically altered beta diversity, taxonomic structure, and function, with reduced microbial network connectivity, which could be involved in the disease etiology.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1112709/fullgastric microbiotaHelicobacter pyloripediatric chronic gastritisnetwork of microbial interactionStreptococcus
spellingShingle Ying Chen
Shou-Yue Xia
Fu-Xia Ru
Jun-Jie Feng
Ji Tao
Zhi-Yuan Wei
Xiu Li
Chengjia Qian
Qiong Lin
Jian-Huan Chen
Gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for Helicobacter pylori
Frontiers in Microbiology
gastric microbiota
Helicobacter pylori
pediatric chronic gastritis
network of microbial interaction
Streptococcus
title Gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for Helicobacter pylori
title_full Gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for Helicobacter pylori
title_fullStr Gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for Helicobacter pylori
title_full_unstemmed Gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for Helicobacter pylori
title_short Gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for Helicobacter pylori
title_sort gastric juice microbiota in pediatric chronic gastritis that clinically tested positive and negative for helicobacter pylori
topic gastric microbiota
Helicobacter pylori
pediatric chronic gastritis
network of microbial interaction
Streptococcus
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1112709/full
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