Fire is a fundamental ecological process. Throughout the history of life on Earth, fire has been a regulatory force that greatly influences ecosystem function and evolution. Its effects are not felt gradually but rather through periodic, sudden, and catastrophic effects on population sizes, community composition, and nutrient cycling (particularly carbon.) Fire's beneficial effects in invigorating ecosystems are well recognized and often put into practice through "prescribed fires." But enormous fires are now an important societal concern. With ever increasing intensity in large part due to climate change, the destructive power of fires is evident worldwide. Whether it is the unrestricted burning of the Amazon rainforest or the wildfires that yearly affect the Western half of North America, the global effects of fires continue to increase. This aerial image (Figure 1) of three major fires burning out of control in California and Oregon this past July make clear the gargantuan size of these catastrophic events. To get a sense of the magnitude and reach of these events, I recommend reading this and this, two New York Times articles with impressive videos included. After the ravaging effects of fire, ecosystems initiate the inevitably much slower process of regeneration, often involving species successions. While much is documented regarding the post-fire establishment of plant and animal species, much less is known about the roles that microbial communities play in ecosystem regeneration. But as STC readers might suspect, it is the microbes that first populate burnt ecosystems. Enter the pyrophilous fungi.
First a brief aside in the style of our customary "Terms in Biology." The term in point is pyrophily: thriving in ground or on material that has recently been scorched or burnt by fire. (Please, never to be confused with the mental disorder pyrophilia.) There are numerous plants and animals said to be pyrophilous, but the clear winners in terms of being the first to thrive in recently burnt areas are the pyrophilous fungi. That some fungi grow well in burnt materials is easy to note. Perhaps some of you have noted filamentous growth of 'fireplace fungi' on the charcoal remaining a few days after lighting a fire in a chimney or in an outdoors grill. One genus of pyrophilous fungi, Pyronema, was so named in 1835 from the Greek πῦρ (pyr) = fire and νῆμᾰ (nêma) = thread. The main character in the paragraphs that follow is Pyronema domesticum (Figure 2). If you look closely at the filamentous growth, you'll notice it is enveloping bits of charcoal, the remains of fire. Pyronema are indeed, true to their namesake, the 'threads after the fire.'
Observations going back more than a century point at P. domesticum (and close relatives) as among the first fungi whose fruiting bodies emerge from recently burned soils. In pre-fire soils this fungus is barely detectable, yet it grows rapidly and robustly in pure culture in the lab. However, early laboratory experiments suggested that Pyronema was a weak competitor in vitro. So what makes it able to quickly take over the soil community post-fires? A recent paper by Monika Fischer and Grace Stark, from Matt Traxler's lab at UC Berkeley, and colleagues provides some exciting answers to this key question. Much prior work already laid a foundation for the more detailed research presented in this paper. For example, the surface composition of recently burnt soils is known to contain a top layer which suffered the highest temperatures and contains mostly completely pyrolyzed organic matter (PyOM). Just below is a "necromass zone" where the heat is not enough to combust organic matter but enough to kill and lyse microbial cells, releasing possible nutrients. Somewhere in that temperature gradient of burning soils there is a "Goldilocks Zone" where the not-too-hot, not-too-cold temperatures allow spores of pyrophilous fungi to survive. Using a pyrocosm model system, Thomas Bruns and colleagues replicated in a controlled environment Pyronema's ability to quickly dominate the fungal community after a fire. The groundwork was thus laid down to ask more detailed questions.
As the Pyronema grow in burnt soils, what nutrients do they use to get that competitive edge? Fischer et al. set out to test the hypothesis that P. domesticum can grow, in part, because they can hydrolyze PyOM. Mind you PyOM is an enormously complex mixture of residual carbon that contains lots of polyaromatic ring residues, not an easy-to-break-down material. It is not even easy to define the structure of PyOM. To obtain charred material in as reproducible a way possible, the authors collaborated with the lab of Thea Whitman in the Soil Science department at the University of Wisconsin, Madison. There, co-authors Nayela Zeba and Timothy Berry used a device called a 'charcoalator' to produce evenly pyrolyzed material at 750°C. This material allowed the authors to carry out elegant if simple growth experiments using different carbon sources. Using sucrose as sole carbon source they observed robust fungal growth, as expected. But they also observed fungal growth when using burnt soil or lab-made PyOM. They then isolated the fungal biomass and performed RNA-Seq analyses to determine the differences in gene expression under the different growth conditions. The first differential response of the fungi growing on PyOM they noticed was the up regulation of genes for transporters and the general stress response. Those fungi, even though they are growing, are showing signs of starvation and stress. But the very interesting observation was that growth on PyOM induced the expression of a coherent set of metabolic pathways involved in aromatic compound degradation (Figure 3). Importantly, they also observed the increased expression of a gene with sequence similarity to bapA, a gene from Aspergillus nidulans whose product oxidizes the polyaromatic hydrocarbon benzo-[a]-pyrene. a carcinogen in humans The product of the orthologous gene in P. domesticum might provide a first step in the breakdown of complex polyaromatic components of PyOM.
The growth on PyOM and the transcription results certainly point to the possibility that P. domesticum can break down this complex substrate. But could the authors prove this directly? Once again, the authors turned to their collaborators in the Whitman lab, who grew a source of wood, seedlings of Pinus strobus (eastern white pine), in a 13CO2 atmosphere for two years. They then pyrolyzed the labeled wood using the charcoalator to generate 13C-PyOM and fed that to P. domesticum. Indeed, they observed the production of 13CO2, proving that P. domesticum directly mineralizes PyOM.
The initial growth of P. domesticum in recently burnt soils is just the beginning of the story. Ecosystem regeneration of course involves the subsequent successions of many other species. What do those late comers grow on? Since P. domesticum's abundance decreases after a few months, it is possible that its biomass serves as a food source in the early stages of succession. This is how the authors speculate on this matter: "Thus, abundant Pyronema biomass may provide a critical nutrient source for secondary colonizers of post-fire soils, thereby laying the foundation for succession within post-fire communities. Importantly, the ability of P. domesticum to convert some PyOM into biomass could directly facilitate the growth of organisms that lack the ability to metabolize PyOM. Thus, Pyronema may provide an important mechanism for rapidly assimilating some portion of newly formed PyOM back into more readily bioavailable forms of carbon in post-fire environments." Once again, fungi prove to be the world's consummate recyclers!
Caption to Figure 3.
Metabolic map highlighting aromatic compound metabolism induced by growth on pyrolyzed substrates. Significantly upregulated genes mapped onto the canonical pathways for aromatic compound metabolism (adjusted value of p<0.01, fold change >2, n=3). Bolded arrows indicate a fold change >8 on PyOM compared to sucrose. Each gene is indicated as a black-outlined box, and the proteins encoded by these genes are indicated as purple text. The color fill of the box indicates the condition(s) in which the gene was upregulated. Multi-colored boxes are slightly larger than mono-color boxes to increase visibility of the colors and to highlight genes that are induced in more than one condition. Diagonal parallel lines within a box and associated dashed lines indicate genes that were expressed, but not differentially expressed under the tested conditions. Source