Helicobacter pylori infection affects the human gastric microbiome, as revealed by metagenomic sequencing

Abstract

Helicobacter pylori infection is a prevalent infectious disease, associated with many gastric diseases, including gastritis, gastric ulcer, and gastric cancer. To reveal the characteristics of the gastric microbiome in patients infected with H. pylori, we performed metagenomic shotgun sequencing of stomach swab samples from 96 patients and then conducted metagenomic association analyses between alterations in the gastric microbiome and H. pylori infection status. The overall composition of the gastric microbiota in H. pylori‐infected individuals was distinctly different from the negative controls; H. pylori became the dominant species after colonizing the human stomach and significantly decreased the α‐diversity of the gastric community (P < 0.05, Wilcoxon rank‐sum test). We also identified 6 HPI‐associated microbial species (FDR < 0.05, Wilcoxon rank‐sum test): Stenotrophomonas maltophilia, Stenotrophomonas unclassified, Chryseobacterium unclassified, Pedobacter unclassified, Variovorax unclassified, and Pseudomonas stutzeri. Furthermore, 55 gastric microbial pathways were enriched in the H. pylori‐positive group, whereas only 2 pathways were more abundant in the H. pylori‐negative group: dTDP‐L‐rhamnose biosynthesis and tetrapyrrole biosynthesis (FDR < 0.05, Wilcoxon rank‐sum test). Gastritis was not associated with non‐H. pylori species in the stomach (P > 0.05, Wilcoxon rank‐sum test). This study revealed alterations in gastric microbial taxa and function associated with HPI in the Chinese population, which provides an insight into gastric microbial interactions and their potential role in the pathological process of gastric diseases.

Microbiome and function alterations in the gastric mucosa of asymptomatic patients with Helicobacter pylori infection

“…39 A number of authors grouped Helicobacter into Proteobacteria in their articles. 14,16 While the Epsilonproteobacteria constitute a stable monophyletic group within the bacterial tree of life, some people suggested that they do not reproducibly affiliate with other Proteobacteria. 39 The expression of non-Helicobacter Proteobacteria appeared to distinguish Helicobacter from Proteobacteria.…”

“…The Epsilonproteobacteria used to be the fifth validly described class of the phylum Proteobacteria, it was widely known for its pathogenic genera Helicobacter 39 . A number of authors grouped Helicobacter into Proteobacteria in their articles 14,16 . While the Epsilonproteobacteria constitute a stable monophyletic group within the bacterial tree of life, some people suggested that they do not reproducibly affiliate with other Proteobacteria 39 .…”

“…Helicobacter pylori is the only bacterium shown to be able to infect the human stomach, common gastrointestinal symptoms including abdominal pain, dyspepsia, belching, and flatulence were thought to be related to H. pylori infection. 3 Studies 6,[13][14][15] have demonstrated that H. pylori infection contributes to gastric microbial dysbiosis, which was perceived as playing a possible role in carcinogenesis. 16,17 The microbial community composition in asymptomatic patients infected with H. pylori yet to be elucidated.…”

The Influence of Helicobacter pylori on Human Gastric and Gut Microbiota

“…In general, in H. pylori -positive subjects, there is an increased abundance of Proteobacteria, likely due to the contribution of H. pylori itself, while the abundance of Actinobacteria, Bacteroidetes, Fusobacteria, and Firmicutes is reduced [ 79 , 81 ]. In a study by Wang et al, some species, such as Stenotrophomonas maltophilia , Chryseobacterium unclassified , Pedobacter unclassified , Stenotrophomonas unclassified , Variovorax unclassified , and Pseudomonas stutzeri , have been associated with the presence of H. pylori infection, through the shotgun sequencing of stomach swab samples of 96 patients [ 82 ]. On the other hand, in a rhesus macaque model, Martin et al observed the impact of H. pylori on the antecedent gastric microbiota and found no significant variations in the relative abundance of non-Helicobacter taxa, indicating that in the rhesus macaque model, the gastric microbiome is stable despite the presence of the H. pylori infection [ 83 ].…”

Relationships among microbiota, gastric cancer, and immunotherapy

“…Other studies have reported the decrease in microbial richness and diversity in GC patients, especially in those with HP ( Ferreira et al, 2018 ; Liu et al, 2019 ). Wang et al (2022) performed metagenomic shotgun sequencing on stomach swab samples from 96 patients with GC, and then conducted metagenomic association analysis between changes in stomach microbiota and HP infection status. It was found that HP became the dominant species after colonization in human stomach, and significantly reduced the α diversity of gastric community.…”