Phosphoribosylpyrophosphate synthetase as a metabolic valve advances Methylobacterium/Methylorubrum phyllosphere colonization and plant growth

Cong Zhang, Di-Fei Zhou, Meng-Ying Wang, Ya-Zhen Song, Chong Zhang, Ming-Ming Zhang, Jing Sun, Lu Yao, Xu-Hua Mo, Zeng-Xin Ma, Xiao-Jie Yuan, Yi Shao, Hao-Ran Wang, Si-Han Dong, Kai Bao, Shu-Huan Lu, Martin Sadilek, Marina G. Kalyuzhnaya, Xin-Hui Xing and Song Yang ()
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Cong Zhang: Qingdao Agricultural University
Di-Fei Zhou: Qingdao Agricultural University
Meng-Ying Wang: Qingdao Agricultural University
Ya-Zhen Song: Qingdao Agricultural University
Chong Zhang: Tsinghua University
Ming-Ming Zhang: Qingdao Agricultural University
Jing Sun: Qingdao Agricultural University
Lu Yao: Chinese Academy of Agricultural Sciences
Xu-Hua Mo: Qingdao Agricultural University
Zeng-Xin Ma: Qingdao Agricultural University
Xiao-Jie Yuan: Qingdao Agricultural University
Yi Shao: Qingdao Agricultural University
Hao-Ran Wang: Qingdao Agricultural University
Si-Han Dong: Qingdao Agricultural University
Kai Bao: Hubei University
Shu-Huan Lu: CABIO Biotech (Wuhan) Co. Ltd.
Martin Sadilek: University of Washington
Marina G. Kalyuzhnaya: San Diego State University
Xin-Hui Xing: Tsinghua University
Song Yang: Qingdao Agricultural University

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract The proficiency of phyllosphere microbiomes in efficiently utilizing plant-provided nutrients is pivotal for their successful colonization of plants. The methylotrophic capabilities of Methylobacterium/Methylorubrum play a crucial role in this process. However, the precise mechanisms facilitating efficient colonization remain elusive. In the present study, we investigate the significance of methanol assimilation in shaping the success of mutualistic relationships between methylotrophs and plants. A set of strains originating from Methylorubrum extorquens AM1 are subjected to evolutionary pressures to thrive under low methanol conditions. A mutation in the phosphoribosylpyrophosphate synthetase gene is identified, which converts it into a metabolic valve. This valve redirects limited C1-carbon resources towards the synthesis of biomass by up-regulating a non-essential phosphoketolase pathway. These newly acquired bacterial traits demonstrate superior colonization capabilities, even at low abundance, leading to increased growth of inoculated plants. This function is prevalent in Methylobacterium/Methylorubrum strains. In summary, our findings offer insights that could guide the selection of Methylobacterium/Methylorubrum strains for advantageous agricultural applications.

Date: 2024
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DOI: 10.1038/s41467-024-50342-9

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