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A widespread response of Gram-negative bacterial acyl-homoserine lactone receptors to Gram-positive Streptomyces γ-butyrolactone signaling molecules

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Abstract

Cell-cell communication is critical for bacterial survival in natural habitats, in which miscellaneous regulatory networks are encompassed. However, elucidating the interaction networks of a microbial community has been hindered by the population complexity. This study reveals that γ-butyrolactone (GBL) molecules from Streptomyces species, the major antibiotic producers, can directly bind to the acyl-homoserine lactone (AHL) receptor of Chromobacterium violaceum and influence violacein production controlled by the quorum sensing (QS) system. Subsequently, the widespread responses of more Gram-negative bacterial AHL receptors to Gram-positive Streptomyces signaling molecules are unveiled. Based on the cross-talk between GBL and AHL signaling systems, combinatorial regulatory circuits (CRC) are designed and proved to be workable in Escherichia coli (E. coli). It is significant that the QS systems of Gram-positive and Gram-negative bacteria can be bridged via native Streptomyces signaling molecules. These findings pave a new path for unlocking the comprehensive cell-cell communications in microbial communities and facilitate the exploitation of innovative regulatory elements for synthetic biology.

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2018YFA0901900 and 2020YFA0907700) and the National Natural Science Foundation of China (31771378 and 31800029). We thank Drs Guomin Ai, Wenzhao Wang, and Jinwei Ren (Institute of Microbiology, Chinese Academy of Sciences, Beijing, China) for assistance with MS and NMR spectroscopy, Luyan Ma (Institute of Microbiology, Chinese Academy of Sciences, Beijing, China) for providing E. coli S17-1 λpir and the plasmid pJN105, and Professor Vittorio Venturi (International Centre for Genetic Engineering and Biotechnology, Trieste, Italy) for the advice on gene disruption in C. violaceum CV12472. We thank Professor Shuishan Song (Biology Institute, Hebei Academy of Sciences, China) for kindly offering C. violaceum CV31532, Professor Junli Zhu (College of Food Science and Biotechnology, Zhejiang Gongshang University, China) for CV026, and Professor Weishan Wang (Institute of Microbiology, Chinese Academy of Sciences, Beijing, China) for plasmids pCS26-Pac and pACYC184. We are grateful to Professor Wenbo Ma (John Innes Centre, Norwich, UK) for the critical reading and helpful suggestions in preparation of the manuscript.

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  1. State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China

    Xiang Liu, Wenxi Wang, Junyue Li, Yue Li, Jihui Zhang & Huarong Tan

  2. College of Life Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China

    Xiang Liu, Wenxi Wang, Junyue Li & Huarong Tan

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  1. Xiang Liu
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  2. Wenxi Wang
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  3. Junyue Li
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Correspondence to Jihui Zhang or Huarong Tan.

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Liu, X., Wang, W., Li, J. et al. A widespread response of Gram-negative bacterial acyl-homoserine lactone receptors to Gram-positive Streptomyces γ-butyrolactone signaling molecules. Sci. China Life Sci. 64, 1575–1589 (2021). https://doi.org/10.1007/s11427-021-1956-8

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