The Development of Aspergillus flavus and Biosynthesis of Aflatoxin B1 are Regulated by the Golgi-Localized Mn2+
Su Qu1, Sheng-Da Chi1, Zhu-Mei He1,2
1School of Life Sciences, Sun Yat-sen University, Guangzhou 510006, China.
Abstract:
Microorganisms rely on diverse ion transport and trace elements to sustain growth, development, and secondary metabolism. Manganese (Mn2+) is essential for various biological processes and plays a crucial role in the metabolism of human cells, plants, and yeast. In Aspergillus flavus, we confirmed that Pmr1 localized in cis- and medial-Golgi compartments was critical in facilitating Mn2+ transport, fungal growth, development, secondary metabolism, and glycosylation. In comparison to the wild type, the Δpmr1 mutant displayed heightened sensitivity to environmental stress, accompanied by inhibited synthesis of aflatoxin B1, kojic acid, and a substantial reduction in pathogenicity toward peanuts and maize. Interestingly, the addition of exogenous Mn2+ effectively rectified the developmental and secondary metabolic defects in the Δpmr1 mutant. However, Mn2+ supplement failed to restore the growth and development of the Δpmr1Δgdt1 double mutant, which indicated that the Gdt1 compensated for the functional deficiency of pmr1. In addition, our results showed that pmr1 knockout leads to an upregulation of O-glycosyl-N-acetylglucose (O-GlcNAc) and O-GlcNAc transferase (OGT), while Mn2+ supplementation can restore the glycosylation in A. flavus. Collectively, this study indicates that the pmr1 regulates Mn2+ via Golgi and maintains growth and metabolism functions of A. flavus through regulation of the glycosylation.
Insights
Pmr1 protein is crucial for manganese transport in Aspergillus flavus, impacting fungal growth, metabolism, and pathogenicity. Supplementing manganese partially rescues defects, but Gdt1 compensates for Pmr1 loss, highlighting complex manganese regulation.
Area of Science:
- Mycology
- Molecular Biology
- Biochemistry
Background:
- Microbial growth, development, and metabolism depend on ion transport and trace elements.
- Manganese (Mn2+) is vital for biological processes across diverse organisms, including fungi.
- The Golgi apparatus plays a key role in cellular ion homeostasis and protein modification.
Purpose of the Study:
- To investigate the role of Pmr1 in manganese (Mn2+) transport and its impact on the growth, development, and secondary metabolism of Aspergillus flavus.
- To elucidate the relationship between Pmr1, manganese homeostasis, and glycosylation pathways in A. flavus.
- To identify potential compensatory mechanisms for Pmr1 function in A. flavus.
Main Methods:
- Gene knockout and double-mutant construction (Δpmr1, Δpmr1Δgdt1).
- Phenotypic analysis of fungal growth, stress sensitivity, and pathogenicity.
- Analysis of secondary metabolite production (aflatoxin B1, kojic acid).
- Assessment of glycosylation patterns, including O-glycosyl-N-acetylglucose (O-GlcNAc) and O-GlcNAc transferase (OGT) expression.
Main Results:
- Pmr1 is localized in the Golgi and essential for Mn2+ transport, fungal growth, development, secondary metabolism, and glycosylation in A. flavus.
- The Δpmr1 mutant exhibits increased stress sensitivity, reduced aflatoxin B1 and kojic acid synthesis, and decreased pathogenicity.
- Exogenous Mn2+ partially restored defects in the Δpmr1 mutant, but not in the Δpmr1Δgdt1 double mutant, indicating Gdt1 compensates for Pmr1.
- Pmr1 knockout upregulates O-GlcNAc and OGT, and Mn2+ supplementation restores glycosylation.
Conclusions:
- Pmr1 regulates Mn2+ transport within the Golgi apparatus of A. flavus.
- Pmr1 is critical for maintaining fungal growth, development, secondary metabolism, and pathogenicity.
- Glycosylation, particularly O-GlcNAc modification, is linked to Mn2+ homeostasis regulated by Pmr1 in A. flavus.
- Gdt1 acts as a functional backup for Pmr1 in manganese transport and homeostasis.
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