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

Abstract

Mega-fires of unprecedented size, intensity, and socio-economic impacts have surged globally due to climate change, fire suppression, and development. Soil microbiomes are critical for post-fire plant regeneration and nutrient cycling, yet how mega-fires impact the soil microbiome remains unclear. We had a serendipitous opportunity to obtain pre- and post-fire soils from the same sampling locations because the 2016 Soberanes Fire, a mega-fire burning >500 Km2, burned with high severity throughout several of our established redwood-tanoak plots. This makes our study the first to examine microbial fire response in redwood-tanoak forests. We re-sampled soils immediately post-fire from two burned plots and one unburned plot to elucidate the effect of mega-fire on soil microbiomes. We used Illumina MiSeq sequencing of 16S and ITS1 to determine that both bacterial and fungal richness were reduced by 38-70% in burned plots, with richness unchanged in the unburned plot. Fire altered composition by 27% for bacteria and 24% for fungi, whereas the unburned plots experienced no change in fungal and negligible change in bacterial composition. We observed several pyrophilous taxa previously observed in Pinaceae forests, indicating that these microbes are likely general fire-responders across forest types. Further, the pyrophilous taxa that positively responded to fire were phylogenetically conserved, suggesting shared evolutionary traits. For bacteria, fire selected for increased Firmicutes and Actinobacteria. For fungi, fire selected for the Ascomycota classes Pezizomycetes and Eurotiomycetes and for a Basidiomycota class of heat-resistant Geminibasidiomycete yeasts. We hypothesize that microbes share analogous fire response to plants and propose a trait-based conceptual model of microbial response to fire that builds from Grimes Competitor-Stress tolerator-Ruderal framework (C-S-R) and its recent applications to microbes. Using this framework and established literature on several microbial species, we hypothesize some generalizable principals to predict which microbial taxa will respond to fire.

Rapid bacterial and fungal successional dynamics in first year after Chaparral wildfire

“…In our system, phosphate was significantly lower in the burned sites (data not shown), thus potentially explaining the fruiting of Coprinellus at later successional stages. Moreover, in support of recent studies in pine forests (Carey et al, 2020;Enright et al, 2021;Pulido-Chavez et al, 2021), we found Geminibasidium in our burned soils. Geminibasidium is a recently described thermotolerant saprobe (H. D. T. Nguyen et al, 2013) that was not present in the unburned sites but dominated early successional stages.…”

“…In bacterial communities, succession and community turnover occurred rapidly and was initiated by aerobic, heterotrophic bacteria that form endospores and produce antibiotics. Consistent with previous studies, these genera belong to the phyla Acidobacteria, Actinobacteria, and Firmicutes (Enright et al, 2021;Whitman et al, 2019). Like plant successional patterns (Capitanio & Carcaillet, 2008;Egler, 1954), early successional stages were characterized by high bacterial diversity and a lack of dominance, mimicking the distributions observed in unburned communities.…”

“…However, Massilia does not form endospores but was nonetheless the most dominant genera post-fire. Massilia is a fast colonizing bacteria, which has been speculated to promote its ability to rapidly colonize the post-fire environment (Enright et al, 2021;Whitman et al, 2019). Together these results suggest that post-fire dominant bacteria in wildfire-adapted systems have coevolved and developed mechanisms to survive the fire resulting in niche exclusion and dominance in recently burned ecosystems.…”

“…In fact, pyrophilous fungi were first discovered over a century ago (Petersen, 1970;Seaver, 1909), and next-generation sequencing has revealed that pyrophilous Ascomycota such as Pyronema can increase 100-fold post-fire (Reazin et al, 2016), dominating over 60% of sequences in the soils of burned pine forest (Bruns et al, 2020). In addition, current studies have provided evidence of pyrophilous bacteria (Enright et al, 2021;Whitman et al, 2019), suggesting that fire resilience and adaptations might be widely distributed within the soil microbial communities. However, we lack an understanding of the fine-scale changes of pyrophilous microbes and their patterns and turnover rates during early secondary succession.…”

“…Wildfire led to a complete turnover of the chaparral soil bacterial and fungal communities favoring pyrophilous bacteria and fungi that have been detected after fires in temperate and boreal forests, such as taxa belonging to the phyla Actinobacteria, Acidobacteria, Firmicutes, and Proteobacteria (Enright et al, 2021;Whitman et al, 2019;Xiang et al, 2014). In particular, the dominance of the genera Massilia, Noviherbaspirillium, and Paenibacillus may be attributed to their ability to survive the wildfire and exploit transient niches in the early post-fire environment.…”