Dynamic interactions within the host-associated microbiota cause tumor formation in the basal metazoan Hydra
Open Access
- 19 March 2020
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLoS Pathogens
- Vol. 16 (3), e1008375
- https://doi.org/10.1371/journal.ppat.1008375
Abstract
The extent to which disturbances in the resident microbiota can compromise an animal’s health is poorly understood. Hydra is one of the evolutionary oldest animals with naturally occurring tumors. Here, we found a causal relationship between an environmental spirochete (Turneriella spec.) and tumorigenesis in Hydra. Unexpectedly, virulence of this pathogen requires the presence of Pseudomonas spec., a member of Hydra´s beneficial microbiome indicating that dynamic interactions between a resident bacterium and a pathogen cause tumor formation. The observation points to the crucial role of commensal bacteria in maintaining tissue homeostasis and adds support to the view that microbial community interactions are essential for disease. These findings in an organism that shares deep evolutionary connections with all animals have implications for our understanding of cancer. Here we follow up on our initial observation of tumor formation in the basal metazoan Hydra and demonstrate that tumor development in one of the evolutionary oldest animals is caused by a dynamic interplay between an environmental spirochete, the host-associated resident microbiota, and the tissue homeostasis within the animal. Unexpectedly, the pathogenicity of the environmental bacterium Turneriella is context-dependent: the virulence of this pathogen requires the presence of a member of Hydra’s beneficial microbiome—the Pseudomonas bacterium. Dynamic interactions between two microbiota members have profound effects onto the host tissue homeostasis and fitness. Our data provide direct evidence for the important role of the resident microbiome in maintaining tissue homeostasis and pathogen defense, a fundamental process that is likely to take place in every tissue of every animal species. In summary, our study uncovers an evolutionary conserved role of the resident microbiome in guarding host’s tissue homeostasis.Keywords
Funding Information
- Deutsche Forschungsgemeinschaft (CRC1182 “Origin and Function of Metaorganisms”)
- Alexander von Humboldt-Stiftung (personal fellowship)
- Canadian Institute for Advanced Research (CIFAR)
This publication has 87 references indexed in Scilit:
- Molecular Signatures of the Three Stem Cell Lineages in Hydra and the Emergence of Stem Cell Function at the Base of MulticellularityMolecular Biology and Evolution, 2012
- Fast gapped-read alignment with Bowtie 2Nature Methods, 2012
- PHAST: A Fast Phage Search ToolNucleic Acids Research, 2011
- antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequencesNucleic Acids Research, 2011
- Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR ampliconsGenome Research, 2011
- In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptidesProceedings of the National Academy of Sciences of the United States of America, 2010
- Search and clustering orders of magnitude faster than BLASTBioinformatics, 2010
- QIIME allows analysis of high-throughput community sequencing dataNature Methods, 2010
- Helicobacter pylori in Health and DiseaseGastroenterology, 2009
- Long-term maintenance of species-specific bacterial microbiota in the basal metazoan HydraProceedings of the National Academy of Sciences of the United States of America, 2007