Trade-off between Plasticity and Velocity in Mycelial Growth

Abstract

Tip-growing fungal cells maintain cell polarity at the apical regions and elongate by de novo synthesis of the cell wall. Cell polarity and tip growth rate affect mycelial morphology. However, it remains unclear how both features act cooperatively to determine cell shape. Here, we investigated this relationship by analyzing hyphal tip growth of filamentous fungi growing inside extremely narrow 1 μm-width channels of microfluidic devices. Since the channels are much narrower than the diameter of hyphae, any hypha growing through the channel must adapt its morphology. Live-cell imaging analyses revealed that hyphae of some species continued growing through the channels, whereas hyphae of other species often ceased growing when passing through the channels, or had lost apical polarity after emerging from the other end of the channel. Fluorescence live-cell imaging analyses of the Spitzenkörper, a collection of secretory vesicles and polarity-related proteins at the hyphal tip, in Neurospora crassa indicates that hyphal tip growth requires a very delicate balance of ordered exocytosis to maintain polarity in spatially confined environments. We analyzed the mycelial growth of seven fungal species from different lineages, including phytopathogenic fungi. This comparative approach revealed that the growth defects induced by the channels were not correlated with their taxonomic classification or with the width of hyphae, but, rather, correlated with the hyphal elongation rate. This report indicates a trade-off between morphological plasticity and velocity in mycelial growth and serves to help understand fungal invasive growth into substrates or plant/animal cells, with direct impact on fungal biotechnology, ecology, and pathogenicity. IMPORTANCE Cell morphology, which is controlled by polarity and growth, is fundamental for all cellular functions. However how polarity and growth act cooperatively to control cell shape remains unclear. Here we investigated their relationship by analyzing hyphal tip growth of filamentous fungi growing inside extremely narrow 1 μm-width channels of microfluidic devices. We found that most fast growing hyphae often lost the cell polarity after emerging from the channels, whereas slow growing hyphae retained polarity and continued growing, indicating a trade-off between plasticity and velocity in mycelial growth. These results serve to understand fungal invasive growth into substrates or plant/animal cells, with direct impact on fungal biotechnology, ecology and pathogenicity.

A Myosin Light Chain Is Critical for Fungal Growth Robustness in Candida albicans

“…This relationship between hyphal diameter and extension rate has been predicted by the vesicle supply center model ( equation 2 ) ( 5 ), and our results establish that this relationship holds upon specific perturbation of the Spitzenkörper. Interestingly, it was recently shown that variation in hyphal width and extension rate increases in faster and wider growing species ( 49 ), suggesting that the regulation of growth may be less precise when growth speeds increase. Together, our results reveal that the Spitzenkörper component Mlc1 links hyphal growth and morphology, suggesting that this structure is critical for minimizing growth and morphology variation in a fungal population, which is likely to be important for mycelium development.…”

From appressorium to transpressorium—Defining the morphogenetic basis of host cell invasion by the rice blast fungus

“…Recent studies in Podospora anserina have, for example, shown that narrow hyphae are developed during fungal growth in order to breach cellulosic substrates such as cellophane [32]. Additionally, recent elegant studies of hyphal morphological adaptation to occupy extremely narrow channels suggest that a trade-off may exist between plasticity and velocity in hyphal growth [33]. These observations provide evidence that generation of specialised hyphae-derived structure for invasive growth may be a conserved mechanism in filamentous fungi.…”

Loss of Septation Initiation Network (SIN) kinases blocks tissue invasion and unlocks echinocandin cidal activity against Aspergillus fumigatus

“…Although human infectious fungi do not utilize special infection structures like appressoria for invasion, the inability of A. fumigatus aseptate hyphae to invade murine lung tissue could be from lack of turgor pressure in the tip compartment required for physical invasion. A recent study exploring the connections between hyphal growth and polarity maintenance has found filamentous fungal organisms with fast growing hyphal tips and high turgor pressure to often lose polarity when undergoing invasive growth (i.e., penetration into small spaces) [77]. in contrast, slow growing fungi with lower turgor pressure are able to maintain a single polarized growth axes under the same conditions.…”