Dual oxidase enables insect gut symbiosis by mediating respiratory network formation
- 9 March 2021
- journal article
- research article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 118 (10)
- https://doi.org/10.1073/pnas.2020922118
Abstract
Most animals harbor a gut microbiota that consists of potentially pathogenic, commensal, and mutualistic microorganisms. Dual oxidase (Duox) is a well described enzyme involved in gut mucosal immunity by the production of reactive oxygen species (ROS) that antagonizes pathogenic bacteria and maintains gut homeostasis in insects. However, despite its nonspecific harmful activity on microorganisms, little is known about the role of Duox in the maintenance of mutualistic gut symbionts. Here we show that, in the bean bug Riptortus pedestris, Duox-dependent ROS did not directly contribute to epithelial immunity in the midgut in response to its mutualistic gut symbiont, Burkholderia insecticola. Instead, we found that the expression of Duox is tracheae-specific and its down-regulation by RNAi results in the loss of dityrosine cross-links in the tracheal protein matrix and a collapse of the respiratory system. We further demonstrated that the establishment of symbiosis is a strong oxygen sink triggering the formation of an extensive network of tracheae enveloping the midgut symbiotic organ as well as other organs, and that tracheal breakdown by Duox RNAi provokes a disruption of the gut symbiosis. Down-regulation of the hypoxia-responsive transcription factor Sima or the regulators of tracheae formation Trachealess and Branchless produces similar phenotypes. Thus, in addition to known roles in immunity and in the formation of dityrosine networks in diverse extracellular matrices, Duox is also a crucial enzyme for tracheal integrity, which is crucial to sustain mutualistic symbionts and gut homeostasis. We expect that this is a conserved function in insects.Keywords
Funding Information
- MEXT | Japan Society for the Promotion of Science (201911493)
- MEXT | Japan Society for the Promotion of Science (20170267)
- MEXT | Japan Society for the Promotion of Science (19J01106)
- Ministry of Education, Culture, Sports, Science and Technology (18KK0211)
- Ministry of Education, Culture, Sports, Science and Technology (20H03303)
This publication has 76 references indexed in Scilit:
- Gene Expression in Gut Symbiotic Organ of Stinkbug Affected by Extracellular Bacterial SymbiontPLOS ONE, 2013
- The unexpected discovery of a novel low-oxygen-activated locus for the anoxic persistence of Burkholderia cenocepaciaThe ISME Journal, 2013
- Trachealess (Trh) regulates all tracheal genes during Drosophila embryogenesisDevelopmental Biology, 2011
- Essential Role of Duox in Stabilization of Drosophila WingOnline Journal of Public Health Informatics, 2011
- Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogasterProceedings of the National Academy of Sciences of the United States of America, 2011
- Perturbed Heme Binding Is Responsible for the Blistering Phenotype Associated with Mutations in the Caenorhabditis elegans Dual Oxidase 1 (DUOX1) Peroxidase DomainOnline Journal of Public Health Informatics, 2010
- Tube continued: morphogenesis of the Drosophila tracheal systemCurrent Opinion in Cell Biology, 2010
- A Peroxidase/Dual Oxidase System Modulates Midgut Epithelial Immunity in Anopheles gambiaeScience, 2010
- Evolution of Mammals and Their Gut MicrobesScience, 2008
- An essential complementary role of NF-κB pathway to microbicidal oxidants in Drosophila gut immunityThe EMBO Journal, 2006