Spontaneous body wall contractions stabilize the fluid microenvironment that shapes host-microbe associations
- Helmholtz Munich, Germany
- Kiel University, Germany
- University of Southern California, United States
Abstract
The freshwater polyp Hydra is a popular biological model system; however, we still do not understand one of its most salient behaviours, the generation of spontaneous body wall contractions. Here, by applying experimental fluid dynamics analysis and mathematical modelling, we provide functional evidence that spontaneous contractions of body walls enhance the transport of chemical compounds from and to the tissue surface where symbiotic bacteria reside. Experimentally, a reduction in the frequency of spontaneous body wall contractions is associated with a changed composition of the colonizing microbiota. Together, our findings suggest that spontaneous body wall contractions create an important fluid transport mechanism that (1) may shape and stabilize specific host-microbe associations and (2) create fluid microhabitats that may modulate the spatial distribution of the colonizing microbes. This mechanism may be more broadly applicable to animal-microbe interactions since research has shown that rhythmic spontaneous contractions in the gastrointestinal tracts are essential for maintaining normal microbiota.
Data availability
All data presented in the main manuscript and supplemental figures is publicly available at NCBI Bioproject PRJNA842888The 16S rRNA sequencing raw data are deposited at the SRA and are available under the project ID PRJNA842888.
Article and author information
Author details
Alexander Klimovich
Funding
Deutsche Forschungsgemeinschaft (CRC 1182 Origin and Function of Metaorganisms"")
- Janna C Nawroth
- Christoph Giez
- Alexander Klimovich
- Eva Kanso
- Thomas CG Bosch
Deutsche Forschungsgemeinschaft (CRC 1461 Neurotronics: Bio-Inspired Information Pathways"")
- Thomas CG Bosch
Deutsche Forschungsgemeinschaft (CRC 1461 Neurotronics: Bio-Inspired Information Pathways"")
- Alexander Klimovich
National Institutes of Health (grant 1 R01 HL 15362201-A)
- Janna C Nawroth
- Christoph Giez
- Alexander Klimovich
- Eva Kanso
National Science Foundation (INSPIRE grant 1608744)
- Janna C Nawroth
- Christoph Giez
- Alexander Klimovich
- Eva Kanso
National Science Foundation (RAISE grant)
- Eva Kanso
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2023, Nawroth et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 654
- views
-
- 107
- downloads
-
- 2
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Spontaneous body wall contractions stabilize the fluid microenvironment that shapes host-microbe associations
eLife 12:e83637.
https://doi.org/10.7554/eLife.83637
Further reading
-
- Physics of Living Systems
Vertebrates have evolved great diversity in the number of segments dividing the trunk body, however, the developmental origin of the evolvability of this trait is poorly understood. The number of segments is thought to be determined in embryogenesis as a product of morphogenesis of the pre-somitic mesoderm (PSM) and the periodicity of a molecular oscillator active within the PSM known as the segmentation clock. Here, we explore whether the clock and PSM morphogenesis exhibit developmental modularity, as independent evolution of these two processes may explain the high evolvability of segment number. Using a computational model of the clock and PSM parameterised for zebrafish, we find that the clock is broadly robust to variation in morphogenetic processes such as cell ingression, motility, compaction, and cell division. We show that this robustness is in part determined by the length of the PSM and the strength of phase coupling in the clock. As previous studies report no changes to morphogenesis upon perturbing the clock, we suggest that the clock and morphogenesis of the PSM exhibit developmental modularity.
-
- Physics of Living Systems
Bacterial biofilms are communities of bacteria usually attached to solid strata and often differentiated into complex structures. Communication across biofilms has been shown to involve chemical signaling and, more recently, electrical signaling in Gram-positive biofilms. We report for the first time, community-level synchronized membrane potential dynamics in three-dimensional Escherichia coli biofilms. Two hyperpolarization events are observed in response to light stress. The first requires mechanically sensitive ion channels (MscK, MscL, and MscS) and the second needs the Kch-potassium channel. The channels mediated both local spiking of single E. coli biofilms and long-range coordinated electrical signaling in E. coli biofilms. The electrical phenomena are explained using Hodgkin-Huxley and 3D fire-diffuse-fire agent-based models. These data demonstrate that electrical wavefronts based on potassium ions are a mechanism by which signaling occurs in Gram-negative biofilms and as such may represent a conserved mechanism for communication across biofilms.
