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

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, Zhoukun Li () and Zhongli Cui ()
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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
Hui Cao: Nanjing Agricultural University
Zhoukun Li: Nanjing Agricultural University
Zhongli Cui: Nanjing Agricultural University

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-41247-0

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