Presentation Information
[4Ferm-13]A spatiotemporal lipid landscape underpins morphogenesis and differentiation in filamentous fungi
○Ryo Iwama1,2 (1. Dept. Biotechnol., UTokyo (Japan), 2. CRIIM, UTokyo (Japan))
Keywords:
filamentous fungi,biological membrane,phospholipid,lipidomics,cellular morphology
Filamentous fungi grow as elongated hyphae and undergo complex developmental transitions from asexual spores (conidia) to hyphal cells and specialized reproductive structures (conidiophores). These morphological changes are important in biotechnology and pathogenesis. Although the mechanisms and regulation of vesicular transport, which is important for hyphal growth, have been well studied, the membrane-level regulation underlying these processes remains largely unexplored.
In this study, we sought to determine the physiological significance of spatiotemporal lipid regulation during fungal development.We performed lipidomics using LC-MS/MS on the model filamentous fungus, Aspergillus nidulans, and detected approximately 500 lipid species. This analysis revealed that lipid composition is not static but undergoes dynamic changes throughout the asexual life cycle. In conidia, phosphatidylcholine (PC) and ubiquinone are predominant; however, as germination progresses and cell polarity is established, there is a marked increase in phosphatidylethanolamine (PE) and highly unsaturated lipid species. These patterns were also evident across distinct colony zones. The colony edge, where tip extension is most active, is enriched with PE and highly unsaturated lipids. Conversely, PC is more abundant in the central region, where conidiophores develop. To examine lipid distribution at higher spatial resolution, we applied Raman microscopy with the initial aim of visualizing membrane phospholipids in situ. Although direct discrimination of individual membrane phospholipid species proved technically challenging, lipid droplets served as an indirect spatial readout of intracellular lipid unsaturation. Raman microscopy focusing on the 1660 cm-1 signal for C=C stretching indicated that triacylglycerols within lipid droplets near hyphal tips were more unsaturated compared to those in older mycelial regions. These results are consistent with the preferential accumulation of unsaturated lipids in tip regions.
Our study also demonstrated that these lipid fluctuations are important for fungal morphogenesis; genetic manipulation of lipid biosynthetic pathways confirmed that changes in PE and PC influence cellular form. A decrease in PE synthesis, achieved through deletion of the phosphatidylserine decarboxylase gene psdB, resulted in a hyperbranching phenotype, indicating that PE helps maintain polarity and suppress excessive branching. Furthermore, in Aspergillus oryzae, we discovered a unique physiological role for PC: while low levels of PC are sufficient for the extension of substrate hyphae within the medium, elevated PC levels are required for aerial differentiation and conidiophore development.
By integrating untargeted lipidomics, Raman spectroscopy, and genetic perturbation of lipid biosynthetic pathways, we revealed that filamentous fungi utilize a lipid landscape to coordinate complex developmental processes.
In this study, we sought to determine the physiological significance of spatiotemporal lipid regulation during fungal development.We performed lipidomics using LC-MS/MS on the model filamentous fungus, Aspergillus nidulans, and detected approximately 500 lipid species. This analysis revealed that lipid composition is not static but undergoes dynamic changes throughout the asexual life cycle. In conidia, phosphatidylcholine (PC) and ubiquinone are predominant; however, as germination progresses and cell polarity is established, there is a marked increase in phosphatidylethanolamine (PE) and highly unsaturated lipid species. These patterns were also evident across distinct colony zones. The colony edge, where tip extension is most active, is enriched with PE and highly unsaturated lipids. Conversely, PC is more abundant in the central region, where conidiophores develop. To examine lipid distribution at higher spatial resolution, we applied Raman microscopy with the initial aim of visualizing membrane phospholipids in situ. Although direct discrimination of individual membrane phospholipid species proved technically challenging, lipid droplets served as an indirect spatial readout of intracellular lipid unsaturation. Raman microscopy focusing on the 1660 cm-1 signal for C=C stretching indicated that triacylglycerols within lipid droplets near hyphal tips were more unsaturated compared to those in older mycelial regions. These results are consistent with the preferential accumulation of unsaturated lipids in tip regions.
Our study also demonstrated that these lipid fluctuations are important for fungal morphogenesis; genetic manipulation of lipid biosynthetic pathways confirmed that changes in PE and PC influence cellular form. A decrease in PE synthesis, achieved through deletion of the phosphatidylserine decarboxylase gene psdB, resulted in a hyperbranching phenotype, indicating that PE helps maintain polarity and suppress excessive branching. Furthermore, in Aspergillus oryzae, we discovered a unique physiological role for PC: while low levels of PC are sufficient for the extension of substrate hyphae within the medium, elevated PC levels are required for aerial differentiation and conidiophore development.
By integrating untargeted lipidomics, Raman spectroscopy, and genetic perturbation of lipid biosynthetic pathways, we revealed that filamentous fungi utilize a lipid landscape to coordinate complex developmental processes.
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