In Vivo Analysis of the Viable Microbiota and Helicobacter pylori Transcriptome in Gastric Infection and Early Stages of Carcinogenesis

Author:

Thorell Kaisa12ORCID,Bengtsson-Palme Johan34,Liu Oscar Hsin-Fu2,Palacios Gonzales Reyna Victoria5,Nookaew Intawat67,Rabeneck Linda8,Paszat Lawrence9,Graham David Y.10,Nielsen Jens6ORCID,Lundin Samuel B.211,Sjöling Åsa12

Affiliation:

1. Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden

2. Department of Microbiology and Immunology, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

3. Department of Infectious Diseases, Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

4. Centre for Antibiotic Resistance Research (CARe), University of Gothenburg, Gothenburg, Sweden

5. Laboratorio de Patología, Hospital Salud Integral, Managua, Nicaragua

6. Department of Biology and Biological Engineering, Chalmers University of Technology, Gothenburg, Sweden

7. Department of Biomedical Informatics, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA

8. Department of Medicine, University of Toronto, and Cancer Care Ontario, Toronto, Ontario, Canada

9. Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada

10. Department of Medicine, Michael E. DeBakey VA Medical Center and Baylor College of Medicine, Houston, Texas, USA

11. Marshall Centre for Infectious Diseases Research and Training, University of Western Australia, Nedlands, Western Australia, Australia

Abstract

ABSTRACT Emerging evidence shows that the human microbiota plays a larger role in disease progression and health than previously anticipated. Helicobacter pylori , the causative agent of gastric cancer and duodenal and gastric ulcers, was early associated with gastric disease, but it has also been proposed that the accompanying microbiota in Helicobacter pylori -infected individuals might affect disease progression and gastric cancer development. In this study, the composition of the transcriptionally active microbial community and H. pylori gene expression were determined using metatranscriptomic RNA sequencing of stomach biopsy specimens from individuals with different H. pylori infection statuses and premalignant tissue changes. The results show that H. pylori completely dominates the microbiota not only in infected individuals but also in most individuals classified as H. pylori uninfected using conventional methods. Furthermore, H. pylori abundance is positively correlated with the presence of Campylobacter , Deinococcus , and Sulfurospirillum . Finally, we quantified the expression of a large number of Helicobacter pylori genes and found high expression of genes involved in pH regulation and nickel transport. Our study is the first to dissect the viable microbiota of the human stomach by metatranscriptomic analysis, and it shows that metatranscriptomic analysis of the gastric microbiota is feasible and can provide new insights into how bacteria respond in vivo to variations in the stomach microenvironment and at different stages of disease progression.

Funder

Assar Gabrielssons Foundation

Swedish Foundation for Strategic Research

Bioinformatics Infrastructure for Life Science

Knut och Alice Wallenbergs Stiftelse

Vetenskapsrådet

VINNOVA

Publisher

American Society for Microbiology

Subject

Infectious Diseases,Immunology,Microbiology,Parasitology

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