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Soil bacterium manipulates antifungal weapons by sensing intracellular type IVA secretion system effectors of a competitor

The ISME Journal volume 17, pages 2232–2246 (2023)Cite this article

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Abstract

Soil beneficial bacteria can effectively inhibit bacterial pathogens by assembling contact-dependent killing weapons, such as the type IVA secretion system (T4ASS). It’s not clear whether these antibacterial weapons are involved in biotrophic microbial interactions in soil. Here we showed that an antifungal antibiotic 2,4-DAPG production of the soil bacterium, Pseudomonas protegens can be triggered by another soil bacterium, Lysobacter enzymogenes, via T4ASS by co-culturing on agar plates to mimic cell-to-cell contact. We demonstrated that the induced 2,4-DAPG production of P. protegens is achieved by intracellular detection of the T4ASS effector protein Le1519 translocated from L. enzymogenes. We defined Le1519 as LtaE (Lysobacter T4E triggering antifungal effects), which specifically stimulates the expression of 2,4-DAPG biosynthesis genes in P. protegens, thereby protecting soybean seedlings from infection by the fungus Rhizoctonia solani. We further found that LtaE directly bound to PhlF, a pathway-specific transcriptional repressor of the 2,4-DAPG biosynthesis, then activated the 2,4-DAPG production. Our results highlight a novel pattern of microbial interspecies and interkingdom interactions, providing a unique case for expanding the diversity of soil microbial interactions.

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Fig. 1: Co-culture of P. protegens and L. enzymogenes on PDA plates triggered interspecies antifungal action.
Fig. 2: P. protegens was activated to inhibit the growth of nearby fungi through intracellular reception/sensing of the L. enzymogenes T4ASS effector LtaE.
Fig. 3: LtaE was a T4E that could be translocated from L. enzymogenes to P. protegens using T4ASS.
Fig. 4: P. protegens activated 2,4-DAPG production through intracellular sensing of LtaE.
Fig. 5: Co-culture of P. protegens and L. enzymogenes or expression of ltaE in P. protegens protected soybean from Rhizoctonia solani infection.
Fig. 6: LtaE directly interacted with PhlF, a pathway-specific transcriptional repressor of 2,4-DAPG biosynthesis.
Fig. 7: LtaE binding alleviated the repressive function of PhlF.

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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), MW052471 (Le1519), MW052474 (Le3316), MW052488 (Le4230), MW052491 (Le4236), MW052493 (Le4253), MW052492 (VirD4).

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Acknowledgements

We thank Prof. Qirong Shen (Nanjing Agricultural University, China) for providing Trichoderma guizhouense NJAU 4742.

Funding

This study was funded by the National Natural Science Foundation of China (U22A20486, 32072470, 31872016 to GQ, and 32272619 to XS), the Natural Key Research and Development Program (2022YFD1400200 to GQ), and Science and technology project of Shanxi Branch of China National Tobacco Corporation (KJ-2022-04 to GQ).

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Authors and Affiliations

  1. College of Plant Protection (State Key Laboratory of Biological interactions and Crop Health; Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing, 210095, P.R. China

    Bingxin Wang, Zeyu Zhang, Fugui Xu, Zixiang Yang, Zihan Li, Danyu Shen, Limin Wang, Huijun Wu, Xiaolong Shao & Guoliang Qian

  2. Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai, 200241, PR China

    Tao Li

  3. Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT, 59717, USA

    Qing Yan

  4. Industrial Crops Institute, Heilongjiang Academy of Agricultural Sciences, Harbin, 150086, China

    Qi Wei

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Contributions

GQ, TL, and XS conceived the project and designed experiments. BW, ZZ, FX, ZY, and ZL carried out experiments. BW, DS, LW, HW, and GQ analyzed data. GQ, TL, QY, QW, and XS wrote and revised the manuscript.

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Correspondence to Guoliang Qian.

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Wang, B., Zhang, Z., Xu, F. et al. Soil bacterium manipulates antifungal weapons by sensing intracellular type IVA secretion system effectors of a competitor. ISME J 17, 2232–2246 (2023). https://doi.org/10.1038/s41396-023-01533-7

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