A team of scientists at the University of Tsukuba, Japan, shed new light on how pathogenic fungi can penetrate tissues by squeezing through tiny gaps between plant and animal cells whereas non-pathogenic fungi do not have this ability.

Fungi are generally described as the scavengers of nature, decomposing and recycling all organic matter. Fungal threads (hyphae) are adept at penetrating through seemingly impenetrable surfaces by extending through tiny gaps that allows them to spread over large areas forming a meshwork of interconnected hyphae called mycelium. How and why hyphae of pathogenic fungal species penetrate through tiny gaps but the hyphae of other fungal species do not, has been unclear.

Fungal plasticity
A team led by the University of Tsukuba has found key differences that explain why some species of fungi can grow successfully through tiny gaps, whereas other fungi–typically those with faster growth rates–cannot squeeze through and stop growing. The trade-off between developmental plasticity and growth rate helps to understand how fungi penetrate surfaces or plant/animal tissues, with important implications for fungal biotechnology, ecology, and studies of disease [University of Tsukuba].
In a new study reported in “Trade-off between Plasticity and Velocity in Mycelial Growth” in the journal mBio, a team led by Norio Takeshita, PhD, professor at the University of Tsukuba with collaborators at Nagoya University in Mexico, has discovered a key feature that helps explain the differences among species of fungi. The researchers compare seven fungi from different taxonomic groups, including some that cause disease in plants.

In this study, the team tests how fungi respond when presented with an obstruction that forces them to pass through very narrow channels. At only one micron wide, the channels of the microfluidic device that the researchers use for their experiments, are narrower than the diameter of fungal hyphae, that are typically two to five microns in different fungal species.

The scientists observe that some fungal species grow readily through the narrow channels, maintaining similar growth rates while extending through the channel, and after emerging from it, as they had before encountering the channel.

In contrast, hyphal mobility in other species almost comes to a halt. The hyphae either stop growing or grow very slowly through the narrow channel. After emerging from the channel, the hyphae often develop a swollen tip. This causes them to lose their sense of direction (depolarization) so that they can no longer maintain their previous growth trajectory.

The authors show hyphae of fungal species such as Aspergillus nidulans and Aspergillus oryzae, pass through the channels but those of a related species Neurospora crassa donot. The authors also show that the rate of hyphal lengthening is much higher in Neurospora crassa than in the other two species that make it through the channel.

The study demonstrates that neither the diameter of the hyphae nor the closeness of their family ties to other pathogenic or non-pathogenic fungal species are factors that contribute to their inability to grow through narrow channels. However, their analysis shows that fungal species with faster growth rates and higher fluid pressure within the cell (turgor pressure) are more likely to show disrupted growth.

Small membrane-bound packages (vesicles) that provide the raw materials—lipids and proteins—needed for assembling boundaries—membranes and cell walls—as hyphae extend, are no longer properly organized during growth through the channel, the researchers report. Labeling live fungi with fluorescent dyes, the team find that vesicles mis-localize inside the cell in the fungi with disrupted growth.

“For the first time, we have shown that there appears to be a trade-off between cell plasticity and growth rate,” says Takeshita. “When a fast-growing hypha passes through a narrow channel, a massive number of vesicles congregate at the point of constriction, rather than passing along to the growing tip. This results in depolarized growth: the tip swells when it exits the channel, and no longer extends. In contrast, a slower growth rate allows hyphae to maintain correct positioning of the cell polarity machinery, permitting growth to continue through the confined space.”

These findings help to understand invasive fungal growth into substrates of plant and animal cells. In addition to its significance from a basic biology standpoint in explaining why certain fungi can penetrate surfaces of living tissues while others cannot, this discovery is also important for future research into fungal biotechnology, ecology and fungal diseases.