A toxin-mediated policing system in Bacillus optimizes division of labor via penalizing cheater-like nonproducers

  1. Rong Huang
  2. Jiahui Shao
  3. Zhihui Xu
  4. Yuqi Chen
  5. Yunpeng Liu
  6. Dandan Wang
  7. Haichao Feng
  8. Weibing Xun
  9. Qirong Shen
  10. Nan Zhang  Is a corresponding author
  11. Ruifu Zhang  Is a corresponding author
  1. Nanjing Agricultural University, China
  2. Chinese Academy of Agricultural Sciences, China
  3. 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.

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All data generated or analysed during this study are included in the manuscript and supporting file.

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Author details

  1. Rong Huang

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Jiahui Shao

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Zhihui Xu

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3987-8836
  4. Yuqi Chen

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yunpeng Liu

    Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Dandan Wang

    College of Resources and Environment, Shandong Agricultural University, Taian, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Haichao Feng

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Weibing Xun

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Qirong Shen

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Nan Zhang

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    For correspondence
    nanzhang@njau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8444-7456
  11. Ruifu Zhang

    Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China
    For correspondence
    rfzhang@njau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.

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.

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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  1. Rong Huang
  2. Jiahui Shao
  3. Zhihui Xu
  4. Yuqi Chen
  5. Yunpeng Liu
  6. Dandan Wang
  7. Haichao Feng
  8. Weibing Xun
  9. Qirong Shen
  10. Nan Zhang
  11. Ruifu Zhang
(2023)
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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https://doi.org/10.7554/eLife.84743

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