A simple pyrocosm for studying soil microbial response to fire reveals a rapid, massive response by Pyronema species

Abstract

We have designed a pyrocosm to enable fine-scale dissection of post-fire soil microbial communities. Using it we show that the peak soil temperature achieved at a given depth occurs hours after the fire is out, lingers near this peak for a significant time, and is accurately predicted by soil depth and the mass of charcoal burned. Flash fuels that produce no large coals were found to have a negligible soil heating effect. Coupling this system with Illumina MiSeq sequencing of the control and post-fire soil we show that we can stimulate a rapid, massive response by Pyronema, a well-known genus of pyrophilous fungus, within two weeks of a test fire. This specific stimulation occurs in a background of many other fungal taxa that do not change noticeably with the fire, although there is an overall reduction in richness and evenness. We introduce a thermo-chemical gradient model to summarize the way that heat, soil depth and altered soil chemistry interact to create a predictable, depthstructured habitat for microbes in post-fire soils. Coupling this model with the temperature relationships found in the pyrocosms, we predict that the width of a survivable "goldilocks zone", which achieves temperatures that select for postfire-adapted microbes, will stay relatively constant across a range of fuel loads. In addition we predict that a larger necromass zone, containing labile carbon and nutrients from recently heat-killed organisms, will increase in size rapidly with addition of fuel and then remain nearly constant in size over a broad range of fuel loads. The simplicity of this experimental system, coupled with the availability of a set of sequenced, assembled and annotated genomes of pyrophilous fungi, offers a powerful tool for dissecting the ecology of post-fire microbial communities. OPEN ACCESSCitation: Bruns TD, Chung JA, Carver AA, Glassman SI (2020) A simple pyrocosm for studying soil microbial response to fire reveals a rapid, massive response by Pyronema species. PLoS ONE 15(3): e0222691. https://doi.

Mega-fire in Redwood Tanoak Forest Reduces Bacterial and Fungal Richness and Selects for Pyrophilous Taxa and Traits that are Phylogenetically Conserved

“…We identified a massive increase in the Basidiomycete yeast Basidioascus and the bacterial Firmicutes post-fire, and we showed that pyrophilous bacteria and fungi and their traits are phylogenetically conserved at the class level. By comparing our work to other recent molecular characterizations of post-fire microbes in Pinaceae forests (Bruns et al, 2020;Glassman et al, 2016;Whitman et al, 2019), we can now begin to generalize traits of post-fire microbes to other forest types and compare them to analogous traits in plants (Figure 7). For example, we hypothesize certain bacteria (Firmicutes) and fungi (Pyronemataceae) appear to be able to survive fire with Mega-Fire Effect on Pyrophilous Microbes 28 thermotolerant structures, and other fungi (Penicillium) or bacteria (Massillia) are fastresponders, and trade-offs might exist among these traits.…”

“…While changes in dominance have been documented in microbial communities post-fire (Pérez-Valera et al, 2018;Whitman et al, 2019), they are at lower levels (2-4% for most abundant taxon) likely because they sampled later after the fire and after the first rains post-fire thus obscuring initial compositional shifts. An experimental fire in laboratory "pyrocosm" (a small-scale highly controlled experimental fire to test the effects of fire on soil samples) similarly found huge increases in dominance with the most abundant taxon Pyronema domesticum occupying 57% of the sequences within 2 weeks of the fire (Bruns et al, 2020). We interpret this level of dominance to indicate the opening of niche space due to massive microbial Mega-Fire Effect on Pyrophilous Microbes 21 death of the pre-fire dominants that allows the few microbial taxa that are thermotolerant or capable of capitalizing on post-fire resources or eating microbial necromass to take over.…”

“…Four of the five fire indicator taxa (Table S6) belong to the Pyronemataceae, which have long been known to fruit extensively after fires (Seaver, 1909). In addition to evidence from fruiting body surveys, the Pyronemataceae genus Pyronema can also dominate belowground mycelium by as much as 60% after experimental laboratory fires (Bruns et al, 2020) and increased 100 fold in frequency after prescribed fires in a P. ponderosa forest (Reazin et al, 2016). Geopyxis alpina was also an indicator of fire, and at least two species of Geopyxis species are known to fruit exclusively on burned soil (Wang et al, 2016).…”

“…Most fire studies use burned areas compared to an unburned control as a substitute for not having pre-fire data from the burned region (Brown et al, 2019; Buscardo et al, 2010; Whitman et al, 2019), laboratory heating experiments (Bruns et al, 2020; Riah-Anglet et al, 2015), or prescribed fire to examine impacts on soil microbes (Brown et al, 2013; Fujimura et al, 2005). While these all provide useful information on microbial response to fire, none of these conditions replicate the size and severity of a mega-fire.…”

Soil Fungal Communities Investigated by Metabarcoding Within Simulated Forensic Burial Contexts

“…Ascomycota are decomposers able to break down the animal tissues into major organic compounds, and they have already been identified as fungal decomposers particularly active during the active decay of the carcass (Metcalf et al, 2016a). Recently, Bruns et al (2020) have postulated that the post-fire microbial habitat is structured by a thermo-chemical gradient, which cause two main effects: a temperature gradient that causes differential mortality with soil depth, and a chemical gradient that structures resources available to recolonizing microbes. On this basis, we can postulate that the rise of temperature originated by the decomposition process in the burial environment that, even if lower than that caused by a fire, is extended in time (e.g., at least 2 months in our study), could cause the same effects, thus leading to the strong presence of fungi belonging to the family Pyronemataceae recorded here.…”