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Siderophore-synthesizing NRPS reprogram lipid metabolic profiles for phenotype and function changes of Arthrobotrys oligospora

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Abstract

The objective of this paper is to explore the function of the AOL-s00215g415 (Aog415) gene, which encodes for the synthesis of siderophore in the nematode trapping fungal model strain A. oligospora, in order to understand the relationship between siderophore biosynthesis and nematode trapping activity. After a through sequence analysis, it was determined that Aog415 is a siderophore-synthesizing NRPS. The product of this gene was then identified to be the hydroxamate siderophore desferriferrichrome, using mass spectrometry analysis. When compared to the WT strains, the Aog415 knockout strain exhibited a 60% decrease in siderophore content in fermentation broth. Additionally, the number of predatory rings of decreased by 23.21%, while the spore yield increased by 37.34%. The deletion of Aog415 did not affect the growth of A. oligospora in diverse nutrient medium. Lipid metabolism-related pathways were the primary targets of Aog415 disruption as revealed by the metabolomic analysis. In comparison to the WT, a significant reduction in the levels of glycerophospholipids, and glycolipids was observed in the mutation. The metabolic alteration in fatty acyls and amino acid-like molecules were significantly disrupted. The knockout of Aog415 impaired the biosynthesis of the hydroxamate siderophore desferriferrichrome, remodeled the flow of fatty acid in A. oligospora, and mainly reprogrammed the membrane lipid metabolism in cells. Desferriferrichrome, a hydroxamate siderophore affects the growth, metabolism and nematode trapping ability of A. oligospora by regulating iron intake and cell membrane homeostasis. Our study uncovered the significant contribution of siderophores to the growth and nematode trapping ability and constructed the relationship among siderophores biosynthesis, lipid metabolism and nematode trapping activity of A. oligospora, which provides a new insight for the development of nematode biocontrol agents based on nematode trapping fungi.

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All supporting dataand protocols have been provided within the article or through supplementary data files. Supplementary material is available with the online version of this article.

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Acknowledgements

This research was funded by the National Natural Science Foundation of China (No. 32200042, 31770066), the Anhui Provincial Natural Science Foundation (No. 2208085QC67), the Natural Science Foundation of Anhui Higher Education Institutions of China (No. KJ2021A0058).

Funding

This article was funded by National Natural Science Foundation of China, no.31770066, no. 32200042, Anhui Provincial Natural Science Foundation,no. 2208085QC67, Natural Science Foundation of Anhui Higher Education Institutions of China, no. KJ2021A0058.

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Contributions

Huiwen Liu, performed the experiments, supported metabolomics analysis, writing (review and editing), supported product identification. Liangyin Sun: performed the experiments, writing. Jintao Zhang supported product identification and manuscript revision, Yongzhong Wang: funding acquisition, supervision, and writing (review and editing). Hengqian Lu: designed the project, investigation, supported metabolomics analysis and data interpretation, writing (review and editing), funding acquisition. All authors discussed the results from the experiments and commented on the manuscript.

Corresponding authors

Correspondence to Yongzhong Wang or Hengqian Lu.

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11274_2023_3840_MOESM1_ESM.docx

Supplementary material 1 (SM1) (WORD): Supplementary Table and FiguresTable S1. Primer sequences used in this study.Figure S1. The phylogenetic tree analysis of Aog415 in A. oligospora.Figure S2. Deletion of Aog415 in A. oligospora.Figure S3. The mirror match showed the matched MS/MS spectrum peak of desferriferrichrome.

11274_2023_3840_MOESM2_ESM.xlsx

Supplementary material 2 (SM2) (EXCEL): Data matrix of metabolomics analysis

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Liu, H., Sun, L., Zhang, J. et al. Siderophore-synthesizing NRPS reprogram lipid metabolic profiles for phenotype and function changes of Arthrobotrys oligospora. World J Microbiol Biotechnol 40, 46 (2024). https://doi.org/10.1007/s11274-023-03840-9

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  • DOI: https://doi.org/10.1007/s11274-023-03840-9

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