Millions of tons of fungal spores are dispersed in the atmosphere every year. These living cells, along with plant spores and pollen grains, may act as nuclei for condensation of water in clouds. Basidiospores released by mushrooms form a significant proportion of these aerosols, particularly above tropical forests. Mushroom spores are discharged from gills by the rapid displacement of a droplet of fluid on the cell surface. This droplet is formed by the condensation of water on the spore surface stimulated by the secretion of mannitol and other hygroscopic sugars. This fluid is carried with the spore during discharge, but evaporates once the spore is airborne. Using environmental electron microscopy, we have demonstrated that droplets reform on spores in humid air. The kinetics of this process suggest that basidiospores are especially effective as nuclei for the formation of large water drops in clouds. Through this mechanism, mushroom spores may promote rainfall in ecosystems that support large populations of ectomycorrhizal and saprotrophic basidiomycetes. Our research heightens interest in the global significance of the fungi and raises additional concerns about the sustainability of forests that depend on heavy precipitation.

Introduction

Million of tons of fungal spores are dispersed in the atmosphere every year [1]. An individual gilled mushroom can release 30,000 basidiospores every second, corresponding to a daily output of billions of microscopic particles [2]. Basidiospores are discharged from the gill surfaces by a catapult mechanism powered by the rapid movement of a drop of fluid over the spore surface (Fig 1). This fluid is called Buller’s drop in tribute to “the Einstein of Mycology,” A. H. R. Buller (1874–1944). Buller’s drop is formed by the condensation of water on the spore surface that is stimulated by the secretion of mannitol and other hygroscopic sugars [3, 4]. Water also condenses on a spot on the adjacent spore surface. The merger of Buller’s drop with this second volume of fluid (the adaxial drop) causes a rapid displacement of the center of mass of the spore. This fluid motion, driven by surface tension, imparts momentum to the spore and it is launched at an initial velocity of up to 1.8 m s-1 [5]. This mechanism was proposed in some detail in the 1980s [6], and verified later by high-speed video recordings [7].

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larger image TIFF original image Download: Fig 1. Schematic showing process of ballistospore discharge. Buller’s drop and the adaxial drop form via condensation of water on the spore surface and their coalescence causes a rapid shift in the center of mass of the spore that is responsible for the launch. https://doi.org/10.1371/journal.pone.0140407.g001

Discharged spores fall in the narrow spaces between the gills and are dispersed in airflow around the mushroom cap. The same discharge mechanism operates in poroid mushrooms, with fertile tubes rather than gills, in mushrooms with spines, and from the great diversity of fruit bodies that form spores on exposed surfaces. Fluid is carried with basidiospores after discharge, but evaporates once the spore is airborne. Mushroom spores are a primary source of mannitol detected in air samples above tropical forests [1]. Using mannitol as a biotracer, Elbert et al. (2007) estimated that 50 million tonnes of spores are dispersed in the atmosphere every year. This biomass is carried by an Avogadroian number of spores, corresponding to an average of 1,000 spores for every square millimeter of Earth’s surface. Other biogenic aerosols include plant spores and pollen grains. These “primary biological aerosol particles” appear to be particularly important in the Amazon Basin, and other densely forested locations, where they may serve as nuclei for cloud formation and precipitation [8]. Details of the hygroscopic behavior of mushroom spores have not been studied previously.

Environmental scanning electron microscopy (ESEM) has been used in a number of experiments to study the condensation of water on pollen and other particles that become aerosolized [9–13]. This technique allows investigators to study the properties of untreated biological samples to preserve natural surface chemistry and to visualize the condensation of water in real time. In the present study, we report ESEM experiments showing that the extraordinary mechanism of spore discharge in mushrooms has a specific effect on water condensation after spores are dispersed in the atmosphere. This suggests that mushroom spores are particularly powerful catalysts for raindrop formation in clouds and contribute to rainfall. This may be an important phenomenon in ecosystems that support large populations of ectomycorrhizal and saprotrophic basidiomycetes. Our research heightens interest in the global significance of the fungi and raises additional concerns about the sustainability of forests that depend on heavy rainfall.