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Quorum quenching by a type IVA secretion system effector

The ISME Journal volume 17, pages 1564–1577 (2023)Cite this article

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Abstract

Proteobacteria primarily utilize acyl-homoserine lactones (AHLs) as quorum-sensing signals for intra-/interspecies communication to control pathogen infections. Enzymatic degradation of AHL represents the major quorum-quenching mechanism that has been developed as a promising approach to prevent bacterial infections. Here we identified a novel quorum-quenching mechanism revealed by an effector of the type IVA secretion system (T4ASS) in bacterial interspecies competition. We found that the soil antifungal bacterium Lysobacter enzymogenes OH11 (OH11) could use T4ASS to deliver the effector protein Le1288 into the cytoplasm of another soil microbiome bacterium Pseudomonas fluorescens 2P24 (2P24). Le1288 did not degrade AHL, whereas its delivery to strain 2P24 significantly impaired AHL production through binding to the AHL synthase PcoI. Therefore, we defined Le1288 as LqqE1 (Lysobacter quorum-quenching effector 1). Formation of the LqqE1-PcoI complex enabled LqqE1 to block the ability of PcoI to recognize/bind S-adenosy-L-methionine, a substrate required for AHL synthesis. This LqqE1-triggered interspecies quorum-quenching in bacteria seemed to be of key ecological significance, as it conferred strain OH11 a better competitive advantage in killing strain 2P24 via cell-to-cell contact. This novel quorum-quenching also appeared to be adopted by other T4ASS-production bacteria. Our findings suggest a novel quorum-quenching that occurred naturally in bacterial interspecies interactions within the soil microbiome by effector translocation. Finally, we presented two case studies showing the application potential of LqqE1 to block AHL signaling in the human pathogen Pseudomonas aeruginosa and the plant pathogen Ralstonia solanacearum.

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Fig. 1: Heterogenous expression of a predicted effector protein LqqE1 of the Lysobacter enzymogenes type IVA secretion system in Pseudomonas fluorescens impaired the AHL production.
Fig. 2: LqqE1 is a T4E that could be translocated into P. fluorescens by L. enzymogenes using the T4ASS.
Fig. 3: Identification of key amino residues responsible for LqqE1 functioning as a quorum-quenching protein.
Fig. 4: LqqE1 targets multiple AHL synthases via physical interactions.
Fig. 5: Binding LqqE1 blocks PcoI to recognize S-adenosy-L-methionine, a substrate required for AHL synthesis.
Fig. 6: The LqqE1-triggered quorum quenching confers L. enzymogenes competitive advantages during co-culture with P. fluorescens.

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Data availability

The sequence data from the present study have been submitted to the NCBI GenBank under the following accession numbers: MW052467 (Le0908), MW052468 (Le0989), MW052469 (Le1288), MW052471 (Le1519), MW052472 (Le1841), MW052473 (Le3180), MW052474 (Le3316), MW052488 (Le4230), MW052489 (Le4232), MW052491 (Le4236), MW052493 (Le4253), MW052494 (Le4579), MW052495 (Le4949), OQ192195 (La0125), OQ192196 (Lg4270), OQ179943 (16s rRNA), OQ192197 (GyrB), OQ192199 (RpoB), and OQ192198 (RpoD).

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Acknowledgements

This study was funded by the Natural Key Research and Development Program (2022YFD1400200 to GQ), followed by the National Natural Science Foundation of China (U22A20486, 32072470, and 31872016 to GQ), Science and technology project of Shanxi Branch of China National Tobacco Corporation (KJ-2022-04), the Fundamental Research Funds for the Central Universities (KJJQ202001, KYT201805, and KYTZ201403 to GQ), and the Jiangsu University advantage discipline construction project (80900246 to XS).

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  1. College of Plant Protection, Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing, China

    Jinxing Liao, Zihan Li, Dan Xiong, Danyu Shen, Limin Wang, Long Lin, Xiaolong Shao & Guoliang Qian

  2. Integrative Microbiology Research Centre, South China Agricultural University, 510642, Guangzhou, People’s Republic of China

    Lisheng Liao

  3. Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, China

    Peng Li

  4. Department of Plant Pathology, China Agricultural University, Beijing, China

    Li-Qun Zhang

  5. Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou, China

    Hai-Hong Wang

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Contributions

GQ and JL conceived the project and designed experiments. JL carried out experiments. JL, ZL, DX, DS, LW, L Liao, and XS analyzed data and prepared figures and tables. JL, GQ, and XS wrote the manuscript. GQ, XS, L Lin, PL, LZ, and HW revised the manuscript. All authors read and approved the final manuscript.

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Liao, J., Li, Z., Xiong, D. et al. Quorum quenching by a type IVA secretion system effector. ISME J 17, 1564–1577 (2023). https://doi.org/10.1038/s41396-023-01457-2

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