Spontaneous body wall contractions stabilize the fluid microenvironment that shapes host-microbe associations
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
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
-
- 605
- views
-
- 104
- downloads
-
- 2
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Microbiology and Infectious Disease
- Physics of Living Systems
Filamentous multicellular cable bacteria perform centimeter-scale electron transport in a process that couples oxidation of an electron donor (sulfide) in deeper sediment to the reduction of an electron acceptor (oxygen or nitrate) near the surface. While this electric metabolism is prevalent in both marine and freshwater sediments, detailed electronic measurements of the conductivity previously focused on the marine cable bacteria (Candidatus Electrothrix), rather than freshwater cable bacteria, which form a separate genus (Candidatus Electronema) and contribute essential geochemical roles in freshwater sediments. Here, we characterize the electron transport characteristics of Ca. Electronema cable bacteria from Southern California freshwater sediments. Current–voltage measurements of intact cable filaments bridging interdigitated electrodes confirmed their persistent conductivity under a controlled atmosphere and the variable sensitivity of this conduction to air exposure. Electrostatic and conductive atomic force microscopies mapped out the characteristics of the cell envelope’s nanofiber network, implicating it as the conductive pathway in a manner consistent with previous findings in marine cable bacteria. Four-probe measurements of microelectrodes addressing intact cables demonstrated nanoampere currents up to 200 μm lengths at modest driving voltages, allowing us to quantify the nanofiber conductivity at 0.1 S/cm for freshwater cable bacteria filaments under our measurement conditions. Such a high conductivity can support the remarkable sulfide-to-oxygen electrical currents mediated by cable bacteria in sediments. These measurements expand the knowledgebase of long-distance electron transport to the freshwater niche while shedding light on the underlying conductive network of cable bacteria.
-
- Computational and Systems Biology
- Physics of Living Systems
B-cell repertoires are characterized by a diverse set of receptors of distinct specificities generated through two processes of somatic diversification: V(D)J recombination and somatic hypermutations. B cell clonal families stem from the same V(D)J recombination event, but differ in their hypermutations. Clonal families identification is key to understanding B-cell repertoire function, evolution and dynamics. We present HILARy (High-precision Inference of Lineages in Antibody Repertoires), an efficient, fast and precise method to identify clonal families from single- or paired-chain repertoire sequencing datasets. HILARy combines probabilistic models that capture the receptor generation and selection statistics with adapted clustering methods to achieve consistently high inference accuracy. It automatically leverages the phylogenetic signal of shared mutations in difficult repertoire subsets. Exploiting the high sensitivity of the method, we find the statistics of evolutionary properties such as the site frequency spectrum and 𝑑𝑁∕𝑑𝑆 ratio do not depend on the junction length. We also identify a broad range of selection pressures spanning two orders of magnitude.