Kool & The Gang − Celebration
by Christoph
Other than the title Kool & The Gang − Celebration suggests, this post is not about the R&B band of past glories and their biggest hit, but instead celebrates the true "cool kids," mushrooms − biologically correct Fungi − and their "hypothermic nature," studied by Cordero et al. (2023).
Figure 1. Wild mushrooms are colder than the surrounding air. Visible images and infrared thermographs of 20 different wild mushrooms in their natural habitat while attached to their natural substrate. (A) Amanita spp.; (B) Pleurotus ostreatus; © Amanita muscaria; (D) Amanita brunnescens; (E) Russula spp.; (F) Boletus separans; (G) Russula spp.; (H) Amanita spp.; (I) Thelephora spp.; (J) Cerrena unicolor; (K) Cantharellus spp.; (l) Russula spp.; (M) Hortiboletus spp; (N) Marasmius capillaris; (O) Coprinellus micaceus; ℗ Lactifluus spp.; (Q–S) unidentified; and (T) Pleurotus ostreatus. Temperature scale bars at the bottom of each thermograph depict °C. The average temperatures of specimens and surroundings are listed in SI Appendix, Table S1. Frontispiece: (D) A. brunnescens. Source
Just take an autumnal walk in the nearest forest, preferably if it has rained well the days before, and take close-up photos of all kinds of mushrooms. When you take photos with an infrared camera, you'll come back with a collection of "blue mushrooms" (Figure 1). This is what Radamés Cordero and colleagues from Arturo Casadevall's lab at Johns Hopkins University, Baltimore MD, USA have done. However, they had not taken a normal infrared camera with them, but a special one that uses digitally recorded spectra to enable what is technically known as thermography. In simple terms, you can think of it as a thermometer that measures and records, as a thermogram, the surface temperature for every point on a surface. To make thermograms visible to the human eye as thermographs, warmer temperatures are usually assigned reddish and colder temperatures bluish colors, corresponding to the intuitive perception of temperature among Westerners (think color codes on faucets). To interpret such thermographs, you need images from a normal camera from the same perspective (a bit pretentious, one could then speak of "correlative infrared/visible light photography").
The 20 wild mushrooms "thermo‑portrayed" in their natural habitat while attached to their natural substrate were basidiomycetes from various families with their typical fruiting bodies (Figure 1, detail in the frontispiece). As can be seen in the thermographs, not only the cap and the gills were "cold," depending on the species 1.4 to 5.9°C colder than the surrounding air, but also the stipes and other above‑ground visible parts (see here a sketch of mushroom anatomy).
What is the − or at least one − reason for this measured coolness of the mushrooms? It turns out that this question has concerned mycologists for some time and was most thoroughly investigated by Husher et al. (1999), who found that "The temperature of cultured fruit bodies of Lentinula edodes and Pleurotus ostreatus fell upon exposure to low velocity airflow, consistent with an evaporative mechanism of cooling. The mechanism of ballistospore discharge characteristic of basidiomycete fungi is dependent on condensation of water from the air surrounding the spores onto the spore surface. The current model for this process predicts that condensation, and therefore spore discharge, is enhanced by cooling of the fruit body." Our Elio, a passionate mycophile − see chapter 19 of his memoirs − mentioned the sophisticated ways of spore dispersal by mushrooms here, here and here in STC.
Figure 2. The thermal landscape of a Penicillium spp. colony. Close-up of a single colony thermograph shows that the coldest temperature appears at its center and the warmest temperature of the surrounding agar appears near the colony edge Source
"Coolness" is not restricted to the Basidiomycota and is equally found in Ascomycota. Cordero et al. cultivated various yeasts and molds in the lab on Petri dishes and obtained "blue" thermographs of varying shades for all of them. Interestingly, they observed that colonies of the psychrophilic ascomycete Cryomyces antarcticus were ~1.1°C colder than surrounding agar when incubated at 15°C but still 0.4°C colder when incubated at 4°C. Apparently, evaporative cooling is still possible at low temperatures as long as there is sufficient hydration for evaporative cooling and a permissive ambient humidity.
The finding of hypothermia among some forty macroscopic and microscopic fungi, and the lower fungal temperatures consistently explained by evapotranspiration, suggests to the authors that relative coldness is a general property of the fungal kingdom. However, it seems a bit audacious to me to generalize on the basis of such a small sample from two of the known five phyla of the kingdom Fungi (Chytridiomycota, Zygomycota, Ascomycota, Basidiomycota, Glomeromycota). To drop some numbers on fungal diversity here, a recent census by Phukhamsakda et al. (2022) revealed ~150,000 described taxa and an estimated 2–11 million species.
Figure 3. Evaporative cooling in yeast and mold colonies. The evidence for evaporative cooling is observed from the condensed water droplets at the lid of the Petri dish on top of the colonies. Visible (Top and Middle) and thermal images (Bottom) of (A) wildtype H99 Cryptococcus neoformans; (Scale bar, 1 cm.); (B) cap59 acapsular mutant of C. neoformans colonies; (Scale bar, 1 cm.), and © normal Penicillium spp.; (Scale bar 3 cm.) Visible images (Middle row) were altered to increase contrast and help visualize water droplets (arrows). Source
Digital thermography offers high spatial resolutions today, down to the millimeter range (see Figure 3) or even to the sub-millimeter range (Figure 2). When Cordero et al. scanned fungal colonies for their "thermal profile," the researchers found something intriguing: Candida albicans, Cryptococcus neoformans, and Penicillium spp. colonies all had a relatively cold center, readily explained by evapotranspiration, while the temperatures of the agar immediately surrounding the colonies were warmer than the colonies or distant agar (Figure 2). To my (limited) knowledge, heat dissipation through metabolic activity has not been studied deeply in fungi, but it is known from cell physiology studies of mammalian cells (see here for the debated "hot mitochondria").
Cordero et al. (2013) also investigated something that microbiologists know all too well from working with bacteria and fungi in the lab: airborne fungal spores − often Penicllium, Aspergillus and also Fusarium − are keen to "contaminate" freshly prepared culture media in Petri dishes and do not spare those stored (or forgotten) in the 8°C refrigerator. A couple of days later, the scientist then gazes at droplets of condensed water above the growing fungal colonies on the inside of the lids (and is careful when removing the droplets from the lids because they are full of spores and make for an excellent inoculum wherever they splash).
The researchers found that such droplets form readily on the inside of the lids of Petri dishes not only with known sporeformers such as Penicillium spp. (Figure 3C), but also in fungi that grow mainly in the yeast form such as Cryptococcus neoformans (Figure 3A). Evaporative cooling was the obvious reason for droplet formation since all three colonies in Figure 3 were measurably colder than the surrounding agar (bottom panel). A detail: the capsule‑positive C. neoformans colony was apparently a tad warmer than the capsule‑negative cap59 mutant colony (Figure 3B). It is known that the C. neoformans polysaccharide capsule is a highly hydrated structure that avidly incorporates and retains water, and such water retention may be limiting the rate of evapotranspiration, resulting in "warmer" colonies.
I wonder what else mycologists will be learning in the future when they listen more carefully to Kool & The Gang, the real ones. And, finally, when you want to comment on this post, We would be happy about it! Please comment on Mastodon, or on Bluesky.
