Phoenicoid fungi, spore dormancy, and new ecological niches exposed by burns

Living in a hot Tennessee climate for the last five summers, I’ve come to appreciate how we as humans deal with ever-increasing summertime temperatures. For residents of some states in the US, these dangerously hot summer temperatures can lead to extreme wildland fires that spread for many miles and damage or destroy thousands of homes. Humans have controlled fire for hundreds of thousands of years but not without great cost. Many famous cities have historically been burned to the ground because of accidents related to the use of fire (checkout the top ten fires in history). While recently thumbing through a copy of Fungal Ecology (Dix and Webster, 1995), I was surprised to discover that fungi are able to make use of fire, one of nature’s deadliest and most incredible forces. Specifically, fire plays a key role in shaping the types of fungi that can inhabit a burned soil as well as promoting the formation of a new generation of fungi in soils subjected to a burn (Reazin et al., 2016; Cowan et al., 2016; Smith et al., 2016). The heat produced by fire can stimulate the activation and germination of some fungi’s spores and changes the physicochemical properties of soil, eventually creating a new niche for some fungal species to thrive (Kipfer et al., 2010; Deacon, 2005). In addition, volatile chemicals are released when carbon-rich plant matter burns, and these chemical cues may also trigger germination of some fungal species. In any case, fungi respond directly or indirectly to both the heat and chemical cues produced by a burn.

Dr. Jumpponen highlighting observed changes to the fungal community two years following a burn (ISME meeting in Montréal, QC, Canada, August 2016).

Dr. Ari Jumpponen (Kansas State University)and collaborators (Kansas State University and Oregon State Univeristy) presented research findings about the little studied phoenicoid fungal communities at the 2016 ISME meeting in Montréal, QC (see photo above). Their now published work (Smith et al., 2016) showed that temperatures can exceed 100 °C down to 10 cm depth (and as high as 700 °C) in soils exposed to a burn. Heat derived from fire is not a trivial stress; too hot and spores will burst or melt in the soil like the sticky black fat plaguing the insides of our kitchen ovens.

So how widespread is this behavior in fungi, what fungal traits are responsible for this behavior, and is responding rapidly to a burned area advantageous? The majority of the described pyrophilous (literally fire-loving) fungi are evolutionarily derived (recent) ascomycete or basidiomycete species that diverged roughly 400-800 million years ago (Berbee and Taylor, 2010). Although this behavior is most often observed in the phyla Ascomycota and Basidiomycota, some evidence suggests that pyrophilous members of the Mucoromycotina exist (Petersen, 1970; Reazin et al., 2016). One of the most recognizable members of pyrophilous fungi frequently found in temperate to subtropical habitats are members of the genus Neurospora. These ascomycete fungi are widely regarded as generalist saprotrophs (feast on decaying material) and contain members that represent model organisms for molecular biological research. Their conspicuous blaze pink or orange conidiophores have been observed on baked or heated confectioneries, charred vegetation or tree bark after wild fires, and even large tracts of accumulated tephra produced after a volcanic eruption (Dix and Webster, 1995; Deacon, 2005; Jacobson et al., 2004; Perkins, 1992). Other ascomycetes like Rhizina and Muciturbo are associated with prolific growth of fruit bodies in soil after burning of coniferous and eucalypt forests of temperate and subtropical regions of the globe, respectively (Deacon, 2005). In order to take advantage of available nutrients and reduced competition following a burn, phoenicoid fungi likely occupy lower or adjacent soil horizons with slightly reduced temperatures since the intense heat from burns would inactivate or damage fungal spores but does not penetrate deeper soil horizons (Reazin et al., 2016).

 

 

 

 

 

 

 

A high intensity fire produced by burning megalogs. Photo provided by Dr. Ari Jumpponen.

Spore dormancy (specifically constitutive dormancy) is likely a key trait contributing to the overall ability of pyrophilous fungi to rapidly respond from adjacent soil areas following a burn. Constitutive dormancy refers to the ability of a spore to maintain dormancy in the presence of environmental cues that would normally allow cell growth (Deacon, 2005). Sexually-derived fungal spores usually display constitutive dormancy, whereas asexual spores are activated by metabolizable nutrient cues and are key to dispersal rather than long term survival in soil. The sporadic nature of temperature fluxuations, spore thickness and permeability, metabolic and chemical self-inhibition, and irregularity of external chemical cues (e.g., furfural produced during fire) could be key factors leading to constitutive dormancy in pyrophilous fungi and allow them to quickly respond following a burn (Griffin, 1994).  As previously mentioned, high soil temperatures produced by burning change both the physical and chemical properties of soil. Overall changes include a decrease in organic matter content of the soil, an increased soil pH (alkaline conditions), and a change in water insoluble fractions of micronutrients (e.g., Ca, Mg, K, P) in the soil (Certini, 2005; Dix and Webster, 1995).  Fungi capable of constitutive dormancy until exposure to high temperature may benefit from early access to readily metabolizable soil nutrients after a burn. Hence, offspring of pyrophilous fungi can rapidly utilize these nutrients, reproduce, and spawn a new generation of dormant spores until another intermittent high temperature event. Furthermore, changes in reflective properties due to dark ash accumulation keep soil temperatures elevated following a burn, suggesting that pyrophilous fungi are also capable of performing well in soils exposed to long term, elevated temperatures (Certini, 2005).

The fruiting body of a Morel mushroom pokes through soil exposed to a burn. Photo courtesy of Dr. Ari Jumpponen.

Although fungi will probably never be heralded as mythical creatures that rise from the fiery ashes like the phoenix, phoenicoid fungi should be praised for their ability to take advantage of one of nature’s most extreme forces. So the next time you’re snuggled up next to that warm cozy campfire, remember that your pyrophilous fungal friends are likely warming up right by the campfire too.

References

Berbee ML, Taylor JW. (2010). Dating the molecular clock in fungi – how close are we? Fungal Biol Rev 24: 1–16.

Certini G. (2005). Effects of fire on properties of forest soils: a review. Oecologia 143: 1–10.

Cowan AD, Smith JE, Fitzgerald SA. (2016). Recovering lost ground: Effects of soil burn intensity on nutrients and ectomycorrhiza communities of ponderosa pine seedlings. For Ecol Manage 378: 160–172.

Deacon JW. (2005). Fungal Biology. 4th ed. Wiley-Blackwell: Hoboken, NJ.

Dix NJ, Webster J. (1995). Fungal Ecology. Chapman & Hall: London.

Griffin DH. (1994). Fungal physiology. 2nd ed. Wiley-Liss, Inc.: New York, New York, USA.

Jacobson DJ, Powell AJ, Dettman JR, Saenz GS, Barton MM, Hiltz MD, et al. (2004). Neurospora in temperate forests of western North America. Mycologia 96: 66–74.

Kipfer T, Egli S, Ghazoul J, Moser B, Wohlgemuth T. (2010). Susceptibility of ectomycorrhizal fungi to soil heating. Fungal Biol 114: 467–472.

Perkins DD. (1992). Neurospora: The organism behind the molecular revolution. Genetics 130: 687–701.

Reazin C, Morris S, Smith JE, Cowan AD, Jumpponen A. (2016). Fires of differing intensities rapidly select distinct soil fungal communities in a northwest US ponderosa pine forest ecosystem. For Ecol Manage 377: 118–127.

Smith, J.E., Cowan, A.D., Fitzgerald, S.A., Brenner, C. (2016) Soil heating during the complete combustion of mega-logs and broadcast burning in the central Oregon pumice soils. Int J Wild Fire. In Press.

Petersen, R.M. (1970) Danish fireplace fungi: An ecological investigation on fungi on burns. Dansk Botanisk Arkiv 27: 1–97.

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