Gut bacterial aggregates as living gels

Version of Record: October 25, 2021
Version of Record: October 22, 2021
Version of Record: October 13, 2021
Accepted Manuscript: September 7, 2021

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Abstract
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Abstract

The spatial organization of gut microbiota influences both microbial abundances and host-microbe interactions, but the underlying rules relating bacterial dynamics to large-scale structure remain unclear. To this end we studied experimentally and theoretically the formation of three-dimensional bacterial clusters, a key parameter controlling susceptibility to intestinal transport and access to the epithelium. Inspired by models of structure formation in soft materials, we sought to understand how the distribution of gut bacterial cluster sizes emerges from bacterial-scale kinetics. Analyzing imaging-derived data on cluster sizes for eight different bacterial strains in the larval zebrafish gut, we find a common family of size distributions that decay approximately as power laws with exponents close to -2, becoming shallower for large clusters in a strain-dependent manner. We show that this type of distribution arises naturally from a Yule-Simons-type process in which bacteria grow within clusters and can escape from them, coupled to an aggregation process that tends to condense the system toward a single massive cluster, reminiscent of gel formation. Together, these results point to the existence of general, biophysical principles governing the spatial organization of the gut microbiome that may be useful for inferring fast-timescale dynamics that are experimentally inaccessible.

Data availability

A table of all bacterial cluster sizes analysed in this study is included in the Supplementary Data File. MATLAB code for simulating the models described in the study is available at https://github.com/rplab/cluster_kinetics

The following previously published data sets were used

(2019) Supplementary Data for "Sublethal antibiotics collapse gut bacterial populations by enhancing aggregation and expulsion," Proceedings of the National Academy of Sciences, 116(43): 21392-21400, 2019.
https://doi.org/10.1073/pnas.1907567116.

https://doi.org/10.1073/pnas.1907567116
(2018) Supplementary Data for "Bacterial Cohesion Predicts Spatial Distribution in the Larval Zebrafish Intestine," Biophysical Journal, 115(11): 2271-2277 (2018).
https://doi.org/10.1016/j.bpj.2018.10.017.

https://doi.org/10.1016/j.bpj.2018.10.017

Article and author information

Author details

Brandon H Schlomann

University of Oregon, Eugene, United States

Competing interests
The authors declare that no competing interests exist.
Raghuveer Parthasarathy

University of Oregon, Eugene, United States

For correspondence
raghu@uoregon.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6006-4749

Funding

National Institutes of Health (P50GM09891)

Brandon H Schlomann
Raghuveer Parthasarathy

National Institutes of Health (P01GM125576)

Brandon H Schlomann
Raghuveer Parthasarathy

National Institutes of Health (F32AI112094)

Brandon H Schlomann
Raghuveer Parthasarathy

National Institutes of Health (T32GM007759)

Raghuveer Parthasarathy

National Science Foundation (1427957)

Brandon H Schlomann
Raghuveer Parthasarathy

James S. McDonnell Foundation

Brandon H Schlomann

Kavli Foundation (Kavli Microbiome Ideas Challenge)

Brandon H Schlomann
Raghuveer Parthasarathy

National Institutes of Health (P01HD22486)

Brandon H Schlomann
Raghuveer Parthasarathy

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The studies that generated the data analyzed in this paper (see cited references) were done in strict accordance with protocols approved by the University of Oregon Institutional Animal Care and Use Committee and following standard protocols.

Copyright

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.