Alterations of gastric mucosal microbiota across different stomach microhabitats in a cohort of 276 patients with gastric cancer

Study information

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/09/27

study design

cross-sectional observational, not case-control

Citation

PMID PubMed identifier for scientific articles.

30584008

DOI Digital object identifier for electronic documents.

10.1016/j.ebiom.2018.12.034

URI

Authors

Liu X, Shao L, Liu X, Ji F, Mei Y, Cheng Y, Liu F, Yan C, Li L, Ling Z

Journal

EBioMedicine

Year

2019

Keywords:

Gastric cancer, Gastric microbiota, Helicobacter pylori, Stomach microhabitat, Tumor microenvironment

BACKGROUND: As part of the tumor microenvironment, the gastric microbiota play vital roles in tumor initiation, progression and metastasis, but stomach microhabitats are not always uniform. We aimed to characterize differences of gastric microbiota in stomach microhabitats associated with gastric cancer (GC) development. METHODS: A cohort of 276 GC patients without preoperative chemotherapy was enrolled retrospectively, and 230 normal, 247 peritumoral and 229 tumoral tissues were obtained for gastric microbiota analysis targeting the 16S rRNA gene by MiSeq sequencing. The microbial diversity and composition, bacterial co-occurrence correlations and predictive functional profiles were compared across different microhabitats. FINDINGS: GC-specific stomach microhabitats, not GC stages or types, determine the composition and diversity of the gastric microbiota. Most notably, bacterial richness was decreased in peritumoral and tumoral microhabitats, and the correlation network of abundant gastric bacteria was simplified in tumoral microhabitat. Helicobacter pylori (HP), Prevotella copri and Bacteroides uniformis were significantly decreased, whereas Prevotella melaninogenica, Streptococcus anginosus and Propionibacterium acnes were increased in tumoral microhabitat. Higher HP colonisation influenced the overall structure of the gastric microbiota in normal and peritumoral microhabitats. PiCRUSt analysis revealed that genes associated with nucleotide transport and metabolism and amino acid transport and metabolism were significantly enriched in tumoral microbiota, while gastric acid secretion was significantly higher in HP positive group of the tumoral microbiota. INTERPRETATION: Our present study provided new insights into the roles of gastric microbiota in different stomach microhabitats in gastric carcinogenesis, especially the pathogenesis of HP. FUND: National Natural Science Foundation of China.

Experiment 1

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Curated date: 2021/01/10

Curator: WikiWorks

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Subjects

Location of subjects

China

Host species Species from which microbiome was sampled (if applicable)

Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Stomach Anterior intestine,Gaster,Mesenteron,Stomach chamber,Ventriculus,Stomach

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology

gastric cancer Ca body - stomach,ca greater curvature of stomach,Ca lesser curvature - stomach,cancer of stomach,gastric cancer,gastric cancer, intestinal,gastric neoplasm,malignant gastric neoplasm,malignant gastric tumor,malignant neoplasm of body of stomach,malignant neoplasm of lesser curve of stomach,malignant neoplasm of stomach,malignant neoplasm of the stomach,malignant stomach neoplasm,malignant tumor of body of stomach,malignant tumor of greater curve of stomach,malignant tumor of lesser curve of stomach,malignant tumor of stomach,malignant tumor of the stomach,stomach cancer

Group 0 name Corresponds to the control (unexposed) group for case-control studies

normal tissues

Group 1 name Corresponds to the case (exposed) group for case-control studies

peritumoral tissues

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

gastric cancer

Group 0 sample size Number of subjects in the control (unexposed) group

230

Group 1 sample size Number of subjects in the case (exposed) group

247

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)

1 month

Lab analysis

Sequencing type

16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene

V3-V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance

Illumina

Statistical Analysis

Statistical test

Mann-Whitney (Wilcoxon)

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)

0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?

Yes

Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment

sex, age

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

decreased

Richness Number of species

decreased

Signature 1

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Curated date: 2021/01/10

Curator: Rimsha Azhar

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Source: Figure 2a, 2c, 2f

Description: Comparison of the relative abundance of dominant bacterial taxa at different levels

Abundance in Group 1: increased abundance in peritumoral tissues

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Pseudomonadota
Helicobacteraceae
Halomonadaceae
Streptococcaceae
Veillonellaceae
Shewanellaceae
Lactobacillaceae
Peptostreptococcaceae
Helicobacter
Halomonas
Streptococcus
Shewanella
Lactobacillus
Veillonella
Methylobacterium
Peptostreptococcus
Selenomonas
Aquabacter
Bacteroides fragilis
Akkermansia muciniphila

Revision editor(s): WikiWorks

Signature 2

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Source: Figure 2a, 2c, 2f

Description: Comparison of the relative abundance of dominant bacterial taxa at different levels

Abundance in Group 1: decreased abundance in peritumoral tissues

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Bacillota
Bacteroidota
Acidobacteriota
Fusobacteriota
Chloroflexota
Oscillospiraceae
Enterobacteriaceae
Prevotellaceae
Sphingomonadaceae
Bacteroidaceae
Bacillaceae
Porphyromonadaceae
Prevotella
Sphingomonas
Faecalibacterium
Pseudomonas
Bacteroides
Bacillus
Fusobacterium
Propionibacterium
Corynebacterium
Phascolarctobacterium
Segatella copri
Bacillus cereus

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Experiment 2

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

peritumoral tissues

Group 1 name Corresponds to the case (exposed) group for case-control studies

tumoral tissues

Group 0 sample size Number of subjects in the control (unexposed) group

247

Group 1 sample size Number of subjects in the case (exposed) group

229

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

increased

Chao1 Abundance-based estimator of species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

increased

Richness Number of species

unchanged

Signature 1

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Curated date: 2021/01/10

Curator: Rimsha Azhar

Revision editor(s): WikiWorks

Source: Figure 2a, 2c, 2f

Description: Comparison of the relative abundance of dominant bacterial taxa at different levels

Abundance in Group 1: increased abundance in tumoral tissues

NCBI	Quality Control	Links
Acidobacteriota
Chloroflexota
Enterobacteriaceae
Prevotellaceae
Lachnospiraceae
Azotobacter group
Prevotella
Pseudomonas
Bacillus
Prevotella melaninogenica
Streptococcus anginosus
Propionibacterium
Bacillus cereus

Revision editor(s): WikiWorks

Signature 2

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Curated date: 2021/01/10

Curator: Rimsha Azhar

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Source: Figure 2a, 2c, 2f

Description: Comparison of the relative abundance of dominant bacterial taxa at different levels

Abundance in Group 1: decreased abundance in tumoral tissues

NCBI	Quality Control	Links
Pseudomonadota
Halomonadaceae
Oscillospiraceae
Sphingobacteriaceae
Shewanellaceae
Porphyromonadaceae
Halomonas
Shewanella
Sphingomonas
Faecalibacterium
Phascolarctobacterium
Helicobacter pylori

Revision editor(s): WikiWorks

Experiment 3

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Curated date: 2021/01/10

Curator: WikiWorks

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

normal tissues

Group 0 sample size Number of subjects in the control (unexposed) group

230

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/09/27

Curated date: 2021/01/10

Curator: Rimsha Azhar

Revision editor(s): WikiWorks

Source: Figure 2a, 2c, 2f

Description: Comparison of the relative abundance of dominant bacterial taxa at different levels

Abundance in Group 1: increased abundance in tumoral tissues

NCBI	Quality Control	Links
Bacillota
Actinomycetota
Fusobacteriota
Veillonellaceae
Lachnospiraceae
Shewanellaceae
Peptostreptococcaceae
Halomonas
Streptococcus
Shewanella
Lactobacillus
Bacillus
Selenomonas
Fusobacterium
Propionibacterium
Corynebacterium
Prevotella melaninogenica
Streptococcus anginosus
Cutibacterium acnes
Akkermansia muciniphila

Revision editor(s): WikiWorks

Signature 2

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Curated date: 2021/01/10

Curator: Rimsha Azhar

Revision editor(s): WikiWorks

Source: Figure 2a, 2c, 2f

Description: Comparison of the relative abundance of dominant bacterial taxa at different levels

Abundance in Group 1: decreased abundance in tumoral tissues

NCBI	Quality Control	Links
Pseudomonadota
Helicobacteraceae
Azotobacter group
Bacteroidaceae
Helicobacter
Sphingomonas
Pseudomonas
Bacteroides
Helicobacter pylori
Segatella copri
Bacteroides uniformis

Revision editor(s): WikiWorks

Experiment 4

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Curated date: 2021/01/10

Curator: WikiWorks

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

early stage normal

Group 1 name Corresponds to the case (exposed) group for case-control studies

early stage tumor

Group 0 sample size Number of subjects in the control (unexposed) group

112

Group 1 sample size Number of subjects in the case (exposed) group

116

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

unchanged

Chao1 Abundance-based estimator of species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

unchanged

Signature 1

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Source: Figure 4k, 4l, 4m, 4n

Description: Early-stage gastric microbiota between normal and tumor samples

Abundance in Group 1: increased abundance in early stage tumor

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Cutibacterium acnes
Streptococcus anginosus

Revision editor(s): Claregrieve1, WikiWorks

Signature 2

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Source: Figure 4k, 4l, 4m, 4n

Description: Early-stage gastric microbiota between normal and tumor samples

Abundance in Group 1: decreased abundance in early stage tumor

NCBI	Quality Control	Links
Segatella copri
Sphingomonas yabuuchiae

Revision editor(s): Claregrieve1, WikiWorks

Experiment 5

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Curated date: 2021/01/10

Curator: WikiWorks

Revision editor(s): WikiWorks

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

early stage peritumor

Group 1 sample size Number of subjects in the case (exposed) group

118

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

unchanged

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/09/27

Curated date: 2021/01/10

Curator: Rimsha Azhar

Revision editor(s): Claregrieve1, WikiWorks

Source: Figure 4k, 4l, 4m, 4n

Description: Early-stage gastric microbiota in normal and peritumor samples

Abundance in Group 1: decreased abundance in early stage peritumor

NCBI	Quality Control	Links
Sphingomonas yabuuchiae

Revision editor(s): Claregrieve1, WikiWorks

Experiment 6

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Curated date: 2021/01/10

Curator: WikiWorks

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

late stage normal

Group 1 name Corresponds to the case (exposed) group for case-control studies

late stage tumor

Group 0 sample size Number of subjects in the control (unexposed) group

118

Group 1 sample size Number of subjects in the case (exposed) group

113

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

unchanged

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/09/27

Curated date: 2021/01/10

Curator: Rimsha Azhar

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Source: Figure 4k, 4l, 4m, 4n

Description: Late-stage gastric microbiota in normal and tumor samples

Abundance in Group 1: increased abundance in late stage tumor

NCBI	Quality Control	Links
Cutibacterium acnes
Streptococcus anginosus

Revision editor(s): Claregrieve1, WikiWorks

Experiment 8

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Curated date: 2021/01/10

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Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

late stage peritumor

Group 1 sample size Number of subjects in the case (exposed) group

129

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

decreased

Signature 1

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/09/27

Curated date: 2021/01/10

Curator: Rimsha Azhar

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Source: Figure 4k, 4l, 4m, 4n

Description: late-stage gastric microbiota in normal vs peritumor samples

Abundance in Group 1: decreased abundance in late stage peritumor

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Segatella copri

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Experiment 9

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

normal HP-

Group 1 name Corresponds to the case (exposed) group for case-control studies

normal HP+

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

normal samples that are H. Pylori positive

Group 0 sample size Number of subjects in the control (unexposed) group

64

Group 1 sample size Number of subjects in the case (exposed) group

166

Lab analysis

Statistical Analysis

Statistical test

LEfSe

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)

Not specified

LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool

2

Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment

age, sex

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

decreased

Signature 1

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Source: Figure 5l, Supp FigS9

Description: Taxonomic difference of gastric mucosal microbiota between histopathological H. pylori (HP+ and HP-) groups of gastric cancer in normal microhabitat

Abundance in Group 1: increased abundance in normal HP+

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Burkholderiales
Massilia
Oxalobacteraceae
Bifidobacteriaceae
Bifidobacterium
Bifidobacteriales
Corynebacterium
Corynebacteriaceae
Actinomycetaceae
Actinomyces
Methylobacterium
Methylobacteriaceae
Lachnospiraceae
Sphingomonadales
Sphingomonas
Sphingomonadaceae
Alphaproteobacteria
Streptococcaceae
Streptococcus
Helicobacteraceae
Helicobacter
Campylobacterales
Campylobacterota
Pseudomonadota

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Signature 2

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Source: Figure 5, Supp FigS9

Description: Taxonomic difference of gastric mucosal microbiota between histopathological H. pylori (HP+ and HP-) groups of gastric cancer in normal microhabitat

Abundance in Group 1: decreased abundance in normal HP+

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Acidaminococcaceae
Alteromonadales
Betaproteobacteria
Blautia
Clostridia
Dialister
Eubacteriales
Faecalibacterium
Bacillota
Gemmiger
Halomonadaceae
Halomonas
Oceanospirillales
Oscillospiraceae
Phascolarctobacterium
Prevotella
Prevotellaceae
Roseburia
Ruminococcus
Shewanella
Shewanellaceae
Lachnospiraceae incertae sedis

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Experiment 10

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

peritumor HP-

Group 1 name Corresponds to the case (exposed) group for case-control studies

peritumor HP+

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

peritumor samples that are H. Pylori positive

Group 0 sample size Number of subjects in the control (unexposed) group

65

Group 1 sample size Number of subjects in the case (exposed) group

182

Lab analysis

Statistical Analysis

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)

0.05

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

unchanged

Simpson Estimator of species richness and species evenness: more weight on species evenness

decreased

Signature 1

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Curator: Rimsha Azhar

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Source: Figure S10

Description: Taxonomic difference of gastric mucosal microbiota between histopathological H. pylori (HP+ and HP-) groups of gastric cancer in peritumor microhabitat

Abundance in Group 1: increased abundance in peritumor HP+

NCBI	Quality Control	Links
Bacillaceae
Bacillales
Bacillus
Campylobacterales
Campylobacterota
Gemella
Helicobacter
Helicobacteraceae
Pseudomonadota
Streptococcaceae
Streptococcus
Bacillales Family X. Incertae Sedis

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Signature 2

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Source: Figure S10

Description: Taxonomic difference of gastric mucosal microbiota between histopathological H. pylori (HP+ and HP-) groups of gastric cancer in peritumor microhabitat

Abundance in Group 1: decreased abundance in peritumor HP+

NCBI	Quality Control	Links
Clostridia
Phascolarctobacterium
Acidaminococcaceae
Eubacteriales
Roseburia
Faecalibacterium
Alistipes
Rikenellaceae
Dialister
Oscillospiraceae
Gemmiger
Megamonas
Bacillus
Lactobacillales
Parabacteroides

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Experiment 11

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

tumor HP-

Group 1 name Corresponds to the case (exposed) group for case-control studies

tumor HP+

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

tumor samples that are H. Pylori positive

Group 0 sample size Number of subjects in the control (unexposed) group

77

Group 1 sample size Number of subjects in the case (exposed) group

152

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

unchanged

Chao1 Abundance-based estimator of species richness

unchanged

Simpson Estimator of species richness and species evenness: more weight on species evenness

unchanged

Signature 1

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/09/27

Curated date: 2021/01/10

Curator: Rimsha Azhar

Revision editor(s): WikiWorks

Source: Figure S11

Description: Taxonomic difference of gastric mucosal microbiota between histopathological H. pylori (HP+ and HP-) groups of gastric cancer in tumor microhabitat

Abundance in Group 1: increased abundance in tumor HP+

NCBI	Quality Control	Links
Staphylococcaceae
Staphylococcus
Bacteroidaceae
Bacteroides
Caulobacterales
Caulobacteraceae
Brevundimonas
Hyphomicrobiales
Alphaproteobacteria
Blautia
Burkholderiales
Massilia
Sphingomonadales
Sphingobacteriaceae
Novosphingobium
Helicobacteraceae
Helicobacter
Campylobacterales
Campylobacterota

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Signature 2

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Curator: Rimsha Azhar

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Source: Figure S11

Description: Taxonomic difference of gastric mucosal microbiota between histopathological H. pylori (HP+ and HP-) groups of gastric cancer in tumor microhabitat

Abundance in Group 1: decreased abundance in tumor HP+

NCBI	Quality Control	Links
Acinetobacter
Moraxellaceae
Ruminococcus
Pseudomonas
Azotobacter group
Pseudomonadales
Betaproteobacteria
Brucellaceae
Sphingomonas
Bifidobacteriales
Bifidobacterium
Bifidobacteriaceae
Pseudomonadota

Revision editor(s): WikiWorks