A toxin-mediated policing system in Bacillus optimizes division of labor via penalizing cheater-like nonproducers
- Nanjing Agricultural University, China
- Chinese Academy of Agricultural Sciences, China
- Shandong Agricultural University, China
Abstract
Division of labor, where subpopulations perform complementary tasks simultaneously within an assembly, characterizes major evolutionary transitions of cooperation in certain cases. Currently, the mechanism and significance of mediating the interaction between different cell types during the division of labor, remain largely unknown. Here, we investigated molecular mechanism and ecological function of a policing system for optimizing the division of labor in Bacillus velezensis SQR9. During biofilm formation, cells differentiated into extracellular matrix (ECM)-producers and cheater-like nonproducers. ECM-producers were also active in the biosynthesis of genomic island-governed toxic bacillunoic acids (BAs) and self-resistance; while the nonproducers were sensitive to this antibiotic and could be partially eliminated. Spo0A was identified to be the co-regulator for triggering both ECM production and BAs synthesis/immunity. Besides its well-known regulation of ECM secretion, Spo0A activates acetyl-CoA carboxylase to produce malonyl-CoA, which is essential for BAs biosynthesis, thereby stimulating BAs production and self-immunity. Finally, the policing system not only excluded ECM-nonproducing cheater-like individuals but also improved the production of other public goods such as protease and siderophore, consequently, enhancing the population stability and ecological fitness under stress conditions and in the rhizosphere. This study provides insights into our understanding of the maintenance and evolution of microbial cooperation.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting file.
Article and author information
Author details
Funding
National Natural Science Foundation of China (31870096)
- Ruifu Zhang
National Natural Science Foundation of China (42090064)
- Qirong Shen
National Natural Science Foundation of China (31972512)
- Zhihui Xu
National Natural Science Foundation of China (32072665)
- Nan Zhang
National Natural Science Foundation of China (32072675)
- Weibing Xun
National Key Research and Development Program of China (2022YFD1901300)
- Nan Zhang
Fundamental Research Funds for the Central Universities (KYZZ2022003)
- Ruifu Zhang
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Karine A Gibbs, University of California, Berkeley, United States
Version history
- Preprint posted: May 14, 2022 (view preprint)
- Received: November 7, 2022
- Accepted: April 24, 2023
- Accepted Manuscript published: April 25, 2023 (version 1)
- Version of Record published: May 10, 2023 (version 2)
Copyright
© 2023, Huang 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.
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A toxin-mediated policing system in Bacillus optimizes division of labor via penalizing cheater-like nonproducers
eLife 12:e84743.
https://doi.org/10.7554/eLife.84743
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