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Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I

Author

Listed:
  • Chengyao Xia

    (Nanjing Agricultural University)

  • Yuqiang Zhao

    (Jiangsu Province and Chinese Academy of Sciences)

  • Lei Zhang

    (Nanjing Agricultural University)

  • Xu Li

    (Nanjing Agricultural University)

  • Yang Cheng

    (Nanjing Agriculture University)

  • Dongming Wang

    (Nanjing Agricultural University)

  • Changsheng Xu

    (Nanjing Agricultural University)

  • Mengyi Qi

    (Nanjing Agricultural University)

  • Jihong Wang

    (Nanjing Agricultural University)

  • Xiangrui Guo

    (Nanjing Agricultural University)

  • Xianfeng Ye

    (Nanjing Agricultural University)

  • Yan Huang

    (Nanjing Agricultural University)

  • Danyu Shen

    (Nanjing Agriculture University)

  • Daolong Dou

    (Nanjing Agriculture University
    Nanjing Agricultural University)

  • Hui Cao

    (Nanjing Agricultural University)

  • Zhoukun Li

    (Nanjing Agricultural University)

  • Zhongli Cui

    (Nanjing Agricultural University
    Nanjing Agricultural University)

Abstract

Public metabolites such as vitamins play critical roles in maintaining the ecological functions of microbial community. However, the biochemical and physiological bases for fine-tuning of public metabolites in the microbiome remain poorly understood. Here, we examine the interactions between myxobacteria and Phytophthora sojae, an oomycete pathogen of soybean. We find that host plant and soil microbes complement P. sojae’s auxotrophy for thiamine. Whereas, myxobacteria inhibits Phytophthora growth by a thiaminase I CcThi1 secreted into extracellular environment via outer membrane vesicles (OMVs). CcThi1 scavenges the required thiamine and thus arrests the thiamine sharing behavior of P. sojae from the supplier, which interferes with amino acid metabolism and expression of pathogenic effectors, probably leading to impairment of P. sojae growth and pathogenicity. Moreover, myxobacteria and CcThi1 are highly effective in regulating the thiamine levels in soil, which is correlated with the incidence of soybean Phytophthora root rot. Our findings unravel a novel ecological tactic employed by myxobacteria to maintain the interspecific equilibrium in soil microbial community.

Suggested Citation

  • Chengyao Xia & Yuqiang Zhao & Lei Zhang & Xu Li & Yang Cheng & Dongming Wang & Changsheng Xu & Mengyi Qi & Jihong Wang & Xiangrui Guo & Xianfeng Ye & Yan Huang & Danyu Shen & Daolong Dou & Hui Cao & Z, 2023. "Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41247-0
    DOI: 10.1038/s41467-023-41247-0
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    References listed on IDEAS

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    1. Zhong Wei & Tianjie Yang & Ville-Petri Friman & Yangchun Xu & Qirong Shen & Alexandre Jousset, 2015. "Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health," Nature Communications, Nature, vol. 6(1), pages 1-9, December.
    2. Shiri Freilich & Raphy Zarecki & Omer Eilam & Ella Shtifman Segal & Christopher S. Henry & Martin Kupiec & Uri Gophna & Roded Sharan & Eytan Ruppin, 2011. "Competitive and cooperative metabolic interactions in bacterial communities," Nature Communications, Nature, vol. 2(1), pages 1-7, September.
    3. Martin T. Croft & Andrew D. Lawrence & Evelyne Raux-Deery & Martin J. Warren & Alison G. Smith, 2005. "Algae acquire vitamin B12 through a symbiotic relationship with bacteria," Nature, Nature, vol. 438(7064), pages 90-93, November.
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    Cited by:

    1. Lige Ma & Yu Luo & Chen Chen & Huan Luo & Shuqi Wang & Yue Yuan & Wenhua Yang & Can Liu & Xulv Cao & Nannan Li, 2023. "Bacterial Strategies for Improving the Yield, Quality, and Adaptability of Oil Crops," Agriculture, MDPI, vol. 14(1), pages 1-29, December.

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