Plant selection initiates alternative successional trajectories in the soil microbial community after disturbance

Abstract

Because interactions between plants and microbial organisms can influence species diversity and rates of nutrient cycling, how plants shape microbial communities is fundamental to understanding the structure of ecosystems. Despite this, the spatial and temporal scales over which plants influence microbial communities is poorly understood, particularly whether past abiotic or biotic legacies strongly constrain microbial community development. We examined biogeochemical cycling and microbial community structure in a coastal landscape where historical patterns of vegetation transition after a large fire in 1995 are well known, allowing us to account for past abiotic and biotic conditions. We found that alternative states in microbial community structure and ecosystem processes emerged under different plant species, regardless of past conditions. Greenhouse studies further demonstrated that these differences arise from direct plant selection of microbes, with selection stronger in roots compared with soils, especially for bacteria. Correlation of microbial community structure with seedling growth rates was also stronger for fungi compared to bacteria. Despite these effects, minimal overlap between seedling and field microbial communities indicates that the effects of initial plant selection are not stable; rather, plant selection initiated alternative successional trajectories after the fire. Using data from a guild where we have abundant natural history information, ectomycorrhizal fungi, we show that greenhouse communities are dominated by ruderal taxa that are also common in the field after the fire and that these ruderal fungi strongly alter spatial patterns in plant–soil feedback, enabling invasion and transformation of soils previously occupied by heterospecific plants, thus potentially acting as keystone mutualists.

Crown‐fire severity is more important than ground‐fire severity in determining soil fungal community development in the boreal forest

“…Correlation between Bray-Curtis pairwise distances of fungal communities in the organic mor layer of logged and unlogged burned plots from the same stand and crown-fire severity index as analysed by GLMs n e e w t e b y t i r a l i m i s s i d d n a d e g g o l n u d e g g o l p lots post-fire chronosequences, ectomycorrhizal fungal richness has been found to increase linearly, concurrent with the recovery of above-ground vegetation (Duhamel et al, 2019;Hart et al, 2005;Yang et al, 2020).…”

“…Ectomycorrhizal fungi are essential for post-fire establishment, growth and survival of trees by improving uptake of limiting nutrients and water (Smith & Read, 2008). Disturbance of the symbiosis may influence seedling establishment and stand structure (Duhamel et al, 2019;Nara, 2006;Simard, 2009) as well as long-term forest fertility and productivity (Clemmensen et al, 2013(Clemmensen et al, , 2015. After a fire, ectomycorrhizal fungi can persist on root tips of surviving trees, or as resistant structures, such as sclerotia or spores in the soil (Baar et al, 1999;Glassman et al, 2015).…”

Three decades post‐reforestation has not led to the reassembly of arbuscular mycorrhizal fungal communities associated with remnant primary forests

“…VTX00225 in the restored forest may be owed to the sensitivity of this genus to abiotic stress, and its affiliation with undisturbed forest habitats (Lenoir, Fontaine, & Lounès‐Hadj Sahraoui, 2016). Due to the high network connectivity of this taxon, its absence in the restored forest may be affecting assembly processes in these communities and in turn, their function (Banerjee, Schlaeppi, & van der Heijden, 2018; Duhamel et al., 2019; Tulloch et al., 2018). However, additional experimental approaches that specifically test effects of this taxon on AM fungal community assembly and function are needed.…”

Ectomycorrhizal fungal diversity decreases in Mediterranean pine forests adapted to recurrent fires

“…Lactarius (Cairney & Chambers, 2013;Taylor & Bruns, 1999) were indicators in HiFi areas. Different climatic pressure and historical fire recurrences might have driven plant-soil feedbacks to different directions and selected species of ECM fungi that respond more efficiently to the new environmental conditions (Duhamel et al, 2019).…”