Fire-associated microbial shifts in soils of western conifer forests with Armillaria root disease

Appl Environ Microbiol. 2024 Nov 4:e0131224. doi: 10.1128/aem.01312-24. Online ahead of print.

Abstract

Fires in coniferous forests throughout the northern United States alter ecosystem processes and ecological communities, including the diversity and composition of microbial communities living in the soil. In addition to its influence on ecosystem processes and functions, the soil microbiome can interact with soilborne pathogens to facilitate or suppress plant disease development. Altering the microbiome composition to promote taxa that inhibit pathogenic activity has been suggested as a management strategy for forest diseases, including Armillaria root disease caused by Armillaria solidipes, which causes growth loss and mortality of conifers. These forest ecosystems are experiencing increased wildfire burn severity that could influence A. solidipes activity and interactions of the soil microbiome with Armillaria root disease. In this research, we examine changes to the soil microbiome following three levels of burn severity in a coniferous forest in northern Idaho, United States, where Armillaria root disease is prevalent. We further determine how these changes correspond to the soil microbiomes associated with the pathogen A. solidipes, and a putatively beneficial species, A. altimontana. At 15-months post-fire, we found significant differences in richness and diversity between bacterial communities associated with unburned and burned areas, yet no significant changes to these metrics were found in fungal communities following fire. However, both bacterial and fungal communities showed compositional changes associated with burn severity, including microbial taxa with altered relative abundance. Further, significant differences in the relative abundance of certain microbial taxa in communities associated with the three burn severity levels overlapped with taxa associated with various Armillaria spp. Following severe burn, we observed a decreased relative abundance of beneficial ectomycorrhizal fungi associated with the microbial communities of A. altimontana, which may contribute to the antagonistic activity of this soil microbial community. Additionally, A. solidipes and associated microbial taxa were found to dominate following high-severity burns, suggesting that severe fires provide suitable environmental conditions for these species. Overall, our results suggest that shifts in the soil microbiome and an associated increase in the activity of A. solidipes following high-severity burns in similar conifer forests may result in priority areas for monitoring and proactive management of Armillaria root disease.

Importance: With its influence on ecosystem processes and functions, the soil microbiome can interact with soilborne pathogens to facilitate or suppress plant disease development. These forest ecosystems are experiencing increased wildfire frequency and burn severity that could influence the fungal root pathogen, Armillaria solidipes, and interactions with the soil microbiome. We examined changes to the soil microbiome following three levels of burn severity, and examined how these changes correspond with A. solidipes, and a putatively beneficial species, A. altimontana. Following severe burn, there was a decreased relative abundance of ectomycorrhizal fungi associated A. altimontana. A. solidipes and associated microbial taxa dominated following high-severity burns, suggesting that severe fires provide suitable environmental conditions for these species. Our results suggest that shifts in the soil microbiome and an associated increase in the activity of A. solidipes following high-severity burns in conifer forests may result in priority areas for monitoring and proactive management of Armillaria root disease.

Keywords: Armillaria altimontana; Armillaria solidipes; ectomycorrhizal fungi; fire; root disease.