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Bacterial cohesion predicts spatial distribution in the larval zebrafish intestine

Brandon H. Schlomann, Travis J. Wiles, Elena S. Wall, Karen Guillemin, Raghuveer Parthasarathy
doi: https://doi.org/10.1101/392316
Brandon H. Schlomann
1Institute of Molecular Biology, University of Oregon, Eugene, Oregon, United States of America
2Department of Physics and Materials Science Institute, University of Oregon, Eugene, Oregon, United States of America
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Travis J. Wiles
1Institute of Molecular Biology, University of Oregon, Eugene, Oregon, United States of America
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Elena S. Wall
1Institute of Molecular Biology, University of Oregon, Eugene, Oregon, United States of America
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Karen Guillemin
1Institute of Molecular Biology, University of Oregon, Eugene, Oregon, United States of America
3Humans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, Ontario M5G 1Z8, Canada
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Raghuveer Parthasarathy
1Institute of Molecular Biology, University of Oregon, Eugene, Oregon, United States of America
2Department of Physics and Materials Science Institute, University of Oregon, Eugene, Oregon, United States of America
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Abstract

Are there general biophysical relationships governing the spatial organization of the gut microbiome? Despite growing realization that spatial structure is important for population stability, inter-bacterial competition, and host functions, it is unclear in any animal gut whether such structure is subject to predictive, unifying rules, or if it results from contextual, species-specific behaviors. To explore this, we used light sheet fluorescence microscopy to conduct a high-resolution comparative study of bacterial distribution patterns throughout the entire intestinal volume of live, larval zebrafish. Fluorescently tagged strains of seven bacterial symbionts, representing six different species native to zebrafish, were each separately mono-associated with animals that had been raised initially germ-free. The strains showed large differences in both cohesion—the degree to which they auto-aggregate—and spatial distribution. We uncovered a striking correlation between each strain’s mean position and its cohesion, whether quantified as the fraction of cells existing as planktonic individuals, the average aggregate size, or the total number of aggregates. Moreover, these correlations held within species as well; aggregates of different sizes localized as predicted from the pan-species observations. Together, our findings indicate that bacteria within the zebrafish intestine are subject to generic processes that organize populations by their cohesive properties. The likely drivers of this relationship, peristaltic fluid flow, tubular anatomy, and bacterial growth and aggregation kinetics, are common throughout animals. We therefore suggest that the framework introduced here, of biophysical links between bacterial cohesion and spatial organization, should be useful for directing explorations in other host-microbe systems, formulating detailed models that can quantitatively map onto experimental data, and developing new tools that manipulate cohesion to engineer microbiome function.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 15, 2018.
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Bacterial cohesion predicts spatial distribution in the larval zebrafish intestine
Brandon H. Schlomann, Travis J. Wiles, Elena S. Wall, Karen Guillemin, Raghuveer Parthasarathy
bioRxiv 392316; doi: https://doi.org/10.1101/392316
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Bacterial cohesion predicts spatial distribution in the larval zebrafish intestine
Brandon H. Schlomann, Travis J. Wiles, Elena S. Wall, Karen Guillemin, Raghuveer Parthasarathy
bioRxiv 392316; doi: https://doi.org/10.1101/392316

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