Ascus function: From squirt guns to ooze tubes.

Unlike the mechanism of ballistospore discharge, which was not solved until the 1980s, the operation of asci as pressurized squirt guns is relatively straightforward and was understood in the nineteenth century. Since then, mycologists have sought to understand how structural adaptations to asci have allowed the ascomycetes to expel spores of different shapes and sizes over distances ranging from a few millimeters to tens of centimeters. These modifications include the use of valves at the tips of asci that maintain ascus pressure and expel spores at the highest speeds, and gelatinous appendages that connect spores after release and create larger projectiles with greater momentum than single spores. Clever experiments in the twentieth century coupled with meticulous microscopic studies led investigators to understand how asci with complicated apical structures worked and mathematical models produced estimates of launch speeds. With the recent application of high-speed video microscopy, these inferences about ascus function have been tested by imaging the motion of spores on a microsecond timescale. These experiments have established that ascospore discharge is the fastest fungal movement and is among the fastest movements in biology. Beginning with the history of the study of asci, this review article explains how asci are pressurized, how spores are released, and how far spores travel after their release. We also consider the efficiency of ascospore discharge relative to the mechanism of ballistospore discharge and examine the way that the squirt gun mechanism has limited the morphological diversity of ascomycete fruit bodies.

Splash and grab: biomechanics of peridiole ejection and function of the funicular cord in bird's nest fungi.

The bird's nest fungi (Basidiomycota, Agaricales) package millions of spores into peridioles that are splashed from their basidiomata by the impact of raindrops. In this study we report new information on the discharge mechanism in Crucibulum and Cyathus species revealed with high-speed video. Peridioles were ejected at speeds of 1-5 m per second utilizing less than 2 % of the kinetic energy in falling raindrops. Raindrops that hit the rim of the basidiome were most effective at ejecting peridioles. The mean angle of ejection varied from 67 to 73° and the peridioles travelled over an estimated maximum horizontal distance of 1 m. Each peridiole carried a cord or funiculus that remained in a condensed form during flight. The cord unravelled when its adhesive surface stuck to a surrounding obstacle and acted as a brake that quickly reduced the velocity of the projectile. In nature, this elaborate mechanism tethers peridioles to vegetation in a perfect location for browsing by herbivores.

Solving the aerodynamics of fungal flight: how air viscosity slows spore motion.

Viscous drag causes the rapid deceleration of fungal spores after high-speed launches and limits discharge distance. Stokes' law posits a linear relationship between drag force and velocity. It provides an excellent fit to experimental measurements of the terminal velocity of free-falling spores and other instances of low Reynolds number motion (Re<1). More complex, non-linear drag models have been devised for movements characterized by higher Re, but their effectiveness for modeling the launch of fast-moving fungal spores has not been tested. In this paper, we use data on spore discharge processes obtained from ultra-high-speed video recordings to evaluate the effects of air viscosity predicted by Stokes' law and a commonly used non-linear drag model. We find that discharge distances predicted from launch speeds by Stokes' model provide a much better match to measured distances than estimates from the more complex drag model. Stokes' model works better over a wide range projectile sizes, launch speeds, and discharge distances, from microscopic mushroom ballistospores discharged at <1 m s(-1) over a distance of <0.1mm (Re<1.0), to macroscopic sporangia of Pilobolus that are launched at >10 m s(-1) and travel as far as 2.5m (Re>100).

How far and how fast can mushroom spores fly? Physical limits on ballistospore size and discharge distance in the Basidiomycota.

Active discharge of basidiospores in most species of Basidiomycota is powered by the rapid movement of a droplet of fluid, called Buller's drop, over the spore surface. This paper is concerned with the operation of the launch mechanism in species with the largest and smallest ballistospores. Aleurodiscus gigasporus (Russulales) produces the largest basidiospores on record. The maximum dimensions of the spores, 34 × 28 µm, correspond to a volume of 14 pL and to an estimated mass of 17 ng. The smallest recorded basidiospores are produced by Hyphodontia latitans (Hymenochaetales). Minimum spore dimensions in this species, 3.5 × 0.5 µm, correspond to a volume of 0.5 fL and mass of 0.6 pg. Neither species has been studied using high-speed video microscopy, but this technique was used to examine ballistospore discharge in species with spores of similar sizes (slightly smaller than A. gigasporus and slightly larger than those of H. latitans). Extrapolation of velocity measurements from these fungi provided estimates of discharge distances ranging from a maximum of almost 2 mm in A. gigasporus to a minimum of 4 µm in H. latitans. These are, respectively, the longest and shortest predicted discharge distances for ballistospores. Limitations to the distances traveled by basidiospores are discussed in relation to the mechanics of the discharge process and the types of fruit-bodies from which the spores are released.

Adaptation of the spore discharge mechanism in the basidiomycota.

BACKGROUND: Spore discharge in the majority of the 30,000 described species of Basidiomycota is powered by the rapid motion of a fluid droplet, called Buller's drop, over the spore surface. In basidiomycete yeasts, and phytopathogenic rusts and smuts, spores are discharged directly into the airflow around the fungal colony. Maximum discharge distances of 1-2 mm have been reported for these fungi. In mushroom-forming species, however, spores are propelled over much shorter ranges. In gilled mushrooms, for example, discharge distances of <0.1 mm ensure that spores do not collide with opposing gill surfaces. The way in which the range of the mechanism is controlled has not been studied previously. METHODOLOGY/PRINCIPAL FINDINGS: In this study, we report high-speed video analysis of spore discharge in selected basidiomycetes ranging from yeasts to wood-decay fungi with poroid fruiting bodies. Analysis of these video data and mathematical modeling show that discharge distance is determined by both spore size and the size of the Buller's drop. Furthermore, because the size of Buller's drop is controlled by spore shape, these experiments suggest that seemingly minor changes in spore morphology exert major effects upon discharge distance. CONCLUSIONS/SIGNIFICANCE: This biomechanical analysis of spore discharge mechanisms in mushroom-forming fungi and their relatives is the first of its kind and provides a novel view of the incredible variety of spore morphology that has been catalogued by traditional taxonomists for more than 200 years. Rather than representing non-selected variations in micromorphology, the new experiments show that changes in spore architecture have adaptive significance because they control the distance that the spores are shot through air. For this reason, evolutionary modifications to fruiting body architecture, including changes in gill separation and tube diameter in mushrooms, must be tightly linked to alterations in spore morphology.

The fastest flights in nature: high-speed spore discharge mechanisms among fungi.

BACKGROUND: A variety of spore discharge processes have evolved among the fungi. Those with the longest ranges are powered by hydrostatic pressure and include "squirt guns" that are most common in the Ascomycota and Zygomycota. In these fungi, fluid-filled stalks that support single spores or spore-filled sporangia, or cells called asci that contain multiple spores, are pressurized by osmosis. Because spores are discharged at such high speeds, most of the information on launch processes from previous studies has been inferred from mathematical models and is subject to a number of errors. METHODOLOGY/PRINCIPAL FINDINGS: In this study, we have used ultra-high-speed video cameras running at maximum frame rates of 250,000 fps to analyze the entire launch process in four species of fungi that grow on the dung of herbivores. For the first time we have direct measurements of launch speeds and empirical estimates of acceleration in these fungi. Launch speeds ranged from 2 to 25 m s(-1) and corresponding accelerations of 20,000 to 180,000 g propelled spores over distances of up to 2.5 meters. In addition, quantitative spectroscopic methods were used to identify the organic and inorganic osmolytes responsible for generating the turgor pressures that drive spore discharge. CONCLUSIONS/SIGNIFICANCE: The new video data allowed us to test different models for the effect of viscous drag and identify errors in the previous approaches to modeling spore motion. The spectroscopic data show that high speed spore discharge mechanisms in fungi are powered by the same levels of turgor pressure that are characteristic of fungal hyphae and do not require any special mechanisms of osmolyte accumulation.