Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing
- Stanford University, United States
- University of Michigan, United States
- University of Wisconsin, United States
- University of California, San Francisco, United States
Abstract
Life in a three-dimensional biofilm is typical for many bacteria, yet little is known about how strains interact in this context. Here, we created essential-gene CRISPRi knockdown libraries in biofilm-forming Bacillus subtilis and measured competitive fitness during colony co-culture with wild type. Partial knockdown of some translation-related genes reduced growth rates and led to out-competition. Media composition led some knockdowns to compete differentially as biofilm versus non-biofilm colonies. Cells depleted for the alanine racemase AlrA died in monoculture but survived in a biofilm-colony co-culture via nutrient sharing. Rescue was enhanced in biofilm-colony co-culture with a matrix-deficient parent, due to a mutualism involving nutrient and matrix sharing. We identified several examples of mutualism involving matrix sharing that occurred in three-dimensional biofilm colonies but not when cultured in two dimensions. Thus, growth in a three-dimensional colony can promote genetic diversity through sharing of secreted factors and may drive evolution of mutualistic behavior.
Data availability
Related scripts and data deposited in Dryad Digital Repository (doi:10.5061/dryad.79cnp5htm). Remaining data generated or analysed during this study is included in the manuscript and supporting files.
-
Three-dimensional biofilm growth supports a mutualism involving matrix and nutrient sharing - related scripts and dataDryad Digital Repository, 10.5061/dryad.79cnp5htm.
Article and author information
Author details
Kerwyn Casey Huang
Funding
Paul G. Allen Foundation (Discovery Center at Stanford on Systems Modeling of Infection)
- Heidi A Arjes
- Kerwyn Casey Huang
National Institutes of Health (K22 Award AI137122)
- Jason Peters
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Arjes 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
-
- 3,427
- views
-
- 447
- downloads
-
- 14
- 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)
Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing
eLife 10:e64145.
https://doi.org/10.7554/eLife.64145
Further reading
-
- Ecology
Tracking wild pigs with GPS devices reveals how their social interactions could influence the spread of disease, offering new strategies for protecting agriculture, wildlife, and human health.
-
- Ecology
- Neuroscience
In nature, animal vocalizations can provide crucial information about identity, including kinship and hierarchy. However, lab-based vocal behavior is typically studied during brief interactions between animals with no prior social relationship, and under environmental conditions with limited ethological relevance. Here, we address this gap by establishing long-term acoustic recordings from Mongolian gerbil families, a core social group that uses an array of sonic and ultrasonic vocalizations. Three separate gerbil families were transferred to an enlarged environment and continuous 20-day audio recordings were obtained. Using a variational autoencoder (VAE) to quantify 583,237 vocalizations, we show that gerbils exhibit a more elaborate vocal repertoire than has been previously reported and that vocal repertoire usage differs significantly by family. By performing gaussian mixture model clustering on the VAE latent space, we show that families preferentially use characteristic sets of vocal clusters and that these usage preferences remain stable over weeks. Furthermore, gerbils displayed family-specific transitions between vocal clusters. Since gerbils live naturally as extended families in complex underground burrows that are adjacent to other families, these results suggest the presence of a vocal dialect which could be exploited by animals to represent kinship. These findings position the Mongolian gerbil as a compelling animal model to study the neural basis of vocal communication and demonstrates the potential for using unsupervised machine learning with uninterrupted acoustic recordings to gain insights into naturalistic animal behavior.
