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Diffusible Signaling Factor, a Quorum-Sensing Molecule, Interferes with and Is Toxic Towards Bdellovibrio bacteriovorus 109J

  • Environmental Microbiology
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Abstract

Bdellovibrio bacteriovorus 109J is a predatory bacterium which lives by predating on other Gram-negative bacteria to obtain the nutrients it needs for replication and survival. Here, we evaluated the effects two classes of bacterial signaling molecules (acyl homoserine lactones (AHLs) and diffusible signaling factor (DSF)) have on B. bacteriovorus 109J behavior and viability. While AHLs had a non-significant impact on predation rates, DSF considerably delayed predation and bdelloplast lysis. Subsequent experiments showed that 50 μM DSF also reduced the motility of attack-phase B. bacteriovorus 109J cells by 50% (38.2 ± 14.9 vs. 17 ± 8.9 μm/s). Transcriptomic analyses found that DSF caused genome-wide changes in B. bacteriovorus 109J gene expression patterns during both the attack and intraperiplasmic phases, including the significant downregulation of the flagellum assembly genes and numerous serine protease genes. While the former accounts for the reduced speeds observed, the latter was confirmed experimentally with 50 μM DSF completely blocking protease secretion from attack-phase cells. Additional experiments found that 30% of the total cellular ATP was released into the supernatant when B. bacteriovorus 109J was exposed to 200 μM DSF, implying that this QS molecule negatively impacts membrane integrity.

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Data Availability

The strains used in this study were Escherichia coli MG1655 (ATCC 700926) and Bdellovibrio bacteriovorus 109J (ATCC 43826). The raw transcriptome data is available in the GEO Database in the National Centers for Biotechnology Information (NCBI) under Accession No. GSE150985.

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Funding

Funding for this project was sponsored by the National Research Foundation of Korea under the Mid-Career Project (Grant No. 2020R1A2C2012158) and the Space Core Technology Development Project (Grant No. 2017M1A3A3A02016642). We appreciate the support.

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Authors and Affiliations

  1. Cleveland Clinic Lerner College of Medicine, Case Western Reserve University, Cleveland, OH, 44195, USA

    Mohammed Dwidar & Naseer Sangwan

  2. Department of Cardiovascular & Metabolic Sciences, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, 44195, USA

    Mohammed Dwidar & Naseer Sangwan

  3. Center for Microbiome and Human Health, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, 44195, USA

    Mohammed Dwidar & Naseer Sangwan

  4. School of Life Sciences, Ulsan National Institute of Science and Technology, 50 UNIST-gil, Ulsan, 44919, Republic of Korea

    Hyochan Jang, Wonsik Mun, Hansol Im, Sora Yoon, Sooin Choi, Dougu Nam & Robert J. Mitchell

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  1. Mohammed Dwidar
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Contributions

MD and RJM conceived the idea; MD, HJ, WM, HI, and SC conducted the experiments; MD and RJM analyzed the data; NS, SY, and DN analyzed the transcriptome; MD, NS, and RJM prepared the manuscript.

Corresponding authors

Correspondence to Mohammed Dwidar, Dougu Nam or Robert J. Mitchell.

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Dwidar, M., Jang, H., Sangwan, N. et al. Diffusible Signaling Factor, a Quorum-Sensing Molecule, Interferes with and Is Toxic Towards Bdellovibrio bacteriovorus 109J. Microb Ecol 81, 347–356 (2021). https://doi.org/10.1007/s00248-020-01585-8

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