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

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 myxobac...

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Autores principales: Xia, Chengyao, Zhao, Yuqiang, Zhang, Lei, Li, Xu, Cheng, Yang, Wang, Dongming, Xu, Changsheng, Qi, Mengyi, Wang, Jihong, Guo, Xiangrui, Ye, Xianfeng, Huang, Yan, Shen, Danyu, Dou, Daolong, Cao, Hui, Li, Zhoukun, Cui, Zhongli
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10499793/
https://www.ncbi.nlm.nih.gov/pubmed/37704617
http://dx.doi.org/10.1038/s41467-023-41247-0
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author Xia, Chengyao
Zhao, Yuqiang
Zhang, Lei
Li, Xu
Cheng, Yang
Wang, Dongming
Xu, Changsheng
Qi, Mengyi
Wang, Jihong
Guo, Xiangrui
Ye, Xianfeng
Huang, Yan
Shen, Danyu
Dou, Daolong
Cao, Hui
Li, Zhoukun
Cui, Zhongli
author_facet Xia, Chengyao
Zhao, Yuqiang
Zhang, Lei
Li, Xu
Cheng, Yang
Wang, Dongming
Xu, Changsheng
Qi, Mengyi
Wang, Jihong
Guo, Xiangrui
Ye, Xianfeng
Huang, Yan
Shen, Danyu
Dou, Daolong
Cao, Hui
Li, Zhoukun
Cui, Zhongli
author_sort Xia, Chengyao
collection PubMed
description 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.
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spelling pubmed-104997932023-09-15 Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I Xia, Chengyao Zhao, Yuqiang Zhang, Lei Li, Xu Cheng, Yang Wang, Dongming Xu, Changsheng Qi, Mengyi Wang, Jihong Guo, Xiangrui Ye, Xianfeng Huang, Yan Shen, Danyu Dou, Daolong Cao, Hui Li, Zhoukun Cui, Zhongli Nat Commun Article 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. Nature Publishing Group UK 2023-09-13 /pmc/articles/PMC10499793/ /pubmed/37704617 http://dx.doi.org/10.1038/s41467-023-41247-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Xia, Chengyao
Zhao, Yuqiang
Zhang, Lei
Li, Xu
Cheng, Yang
Wang, Dongming
Xu, Changsheng
Qi, Mengyi
Wang, Jihong
Guo, Xiangrui
Ye, Xianfeng
Huang, Yan
Shen, Danyu
Dou, Daolong
Cao, Hui
Li, Zhoukun
Cui, Zhongli
Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I
title Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I
title_full Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I
title_fullStr Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I
title_full_unstemmed Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I
title_short Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I
title_sort myxobacteria restrain phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase i
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10499793/
https://www.ncbi.nlm.nih.gov/pubmed/37704617
http://dx.doi.org/10.1038/s41467-023-41247-0
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