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Predation of oomycetes by myxobacteria via a specialized CAZyme system arising from adaptive evolution

The ISME Journal volume 17, pages 1089–1103 (2023)Cite this article

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Abstract

As social micropredators, myxobacteria are studied for their abilities to prey on bacteria and fungi. However, their predation of oomycetes has received little attention. Here, we show that Archangium sp. AC19 secretes a carbohydrate-active enzyme (CAZyme) cocktail during predation on oomycetes Phytophthora. These enzymes include three specialized β-1,3-glucanases (AcGlu13.1, –13.2 and –13.3) that act as a cooperative consortium to target β-1,3-glucans of Phytophthora. However, the CAZymes showed no hydrolytic effects on fungal cells, even though fungi contain β-1,3-glucans. Heterologous expression of AcGlu13.1, –13.2 or –13.3 enzymes in Myxococcus xanthus DK1622, a model myxobacterium that antagonizes but does not predate on P. sojae, conferred a cooperative and mycophagous ability that stably maintains myxobacteria populations as a mixture of engineered strains. Comparative genomic analyses suggest that these CAZymes arose from adaptive evolution among Cystobacteriaceae myxobacteria for a specific prey killing behavior, whereby the presence of Phytophthora promotes growth of myxobacterial taxa by nutrient release and consumption. Our findings demonstrate that this lethal combination of CAZymes transforms a non-predatory myxobacterium into a predator with the ability to feed on Phytophthora, and provides new insights for understanding predator-prey interactions. In summary, our work extends the repertoire of myxobacteria predatory strategies and their evolution, and suggests that these CAZymes can be engineered as a functional consortium into strains for biocontrol of Phytophothora diseases and hence crop protection.

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Fig. 1: Biocontrol of P. sojae by Archangium sp. AC19.
Fig. 2: Cell wall decomposition of P. sojae by AC19 and SUP.
Fig. 3: Binding affinity of AcGlu13.1, -13.2 and A-13.3 to cell wall material.
Fig. 4: Homologous sequence analysis of the core CAZymes from AC19 secretory SUP.
Fig. 5: AcGlu13.1, -13.2 and -13.3 degrade cell walls of P. sojae and reduce virulence.
Fig. 6: Essential roles of AcGlu13.1, -13.2 and -13.3 in the predation of P. sojae by a heterologous myxobacterium.
Fig. 7: Cooperative predation of P. sojae by M. xanthus engineered with a multi-enzyme system.
Fig. 8: Predation of P. sojae among Cystobacteraceae is correlated with the presence of the specialized glucanase consortium.

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Acknowledgements

We thank Professor Daolong Dou and Suomeng Dong (Nanjing Agricultural University) for generously providing Phytophthora strains, Assistant Professor Danyu Shen (Nanjing Agricultural University) and Junjun Wu (Jiangnan University) for genome analysis, and Assistant Professor Xu Han (Tianjin Institute of Industrial Biotechnology Chinese Academy of Sciences) for protein structure predictions. This work was supported by the National Natural Science Foundation of China (32070027 to ZL, 32170123 to ZC and 32270066 to ZL), the Key Research & Development Plan of Jiangsu Province (BE2020340 to ZC), the National Science and Technology Major Project (2020ZX08009-04B to ZC), the National Key Research and Development Program of China (2021YFC2103600 to ZC and ZL) and the Fundamental Research Funds for the Central Universities (KYZZ2022001 to ZL). We also thank Mr. Gang Hu and Chun Qin (Electron Microscope Experimental Center, College of Life Sciences, Nanjing Agricultural University) for their help with SEM.

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  1. Key Laboratory of Agricultural Environmental Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Lei Zhang, Chaonan Dong, Jihong Wang, Juying Wang, Lin Liu, Chengyao Xia, Lingli Zhong, Xianfeng Ye, Yan Huang, Hui Cao, Zhoukun Li & Zhongli Cui

  2. The Key Laboratory of Monitoring and Management of Plant Diseases ansingled Insects of Ministry of Agriculture and Rural Affairs, College of Plant Protection, Nanjing Agriculture University, Nanjing, 210095, China

    Muxing Liu, Jiexiong Hu, Xinyu Liu & Jiaqin Fan

  3. Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China

    Yuqiang Zhao

  4. State Key Laboratory of Microbial Technology, Institute of Microbial Technology, Shandong University, Qingdao, China

    Jingjing Wang & Yuezhong Li

  5. Department of Molecular Biology, University of Wyoming, 1000 E University Avenue, Laramie, WY, 82071, USA

    Daniel Wall

  6. Key Laboratory of Biological Interaction and Crop Health, Nanjing Agricultural University, Nanjing, 210095, China

    Zhongli Cui

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Contributions

Z.L., L.Z., and Z.C. designed the experiments; L.Z. performed the majority of the experiments and data interpretation. JHW and CD expressed enzymes and performed pot experiments. ML, JYW, JH and XL performed binding and infection assays; LL, CX and LLZ. helped with experiments. XY and YH analyzed the data; JJW, YL and DW contributed in myxobacterial isolates, evolutionary analysis and manuscript edits. LZ, ZKL and ZC wrote and revised the manuscript.

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Correspondence to Zhoukun Li or Zhongli Cui.

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Zhang, L., Dong, C., Wang, J. et al. Predation of oomycetes by myxobacteria via a specialized CAZyme system arising from adaptive evolution. ISME J 17, 1089–1103 (2023). https://doi.org/10.1038/s41396-023-01423-y

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