Microbiome assembly in thawing permafrost and its feedbacks to climate

Abstract

The physical and chemical changes that accompany permafrost thaw directly influence the microbial communities that mediate the decomposition of formerly frozen organic matter, leading to uncertainty in permafrost-climate feedbacks. Although changes to microbial metabolism and community structure are documented following thaw, the generality of post-thaw assembly patterns across permafrost soils of the world remains uncertain, limiting our ability to predict biogeochemistry and microbial community responses to climate change. Based on our review of the Arctic microbiome, permafrost microbiology, and community ecology, we propose that Assembly Theory provides a framework to better understand thaw-mediated microbiome changes and the implications for community function and climate feedbacks. This framework posits that the prevalence of deterministic or stochastic processes indicates whether the community is well-suited to thrive in changing environmental conditions. We predict that on a short timescale and following high-disturbance thaw (e.g., thermokarst), stochasticity dominates post-thaw microbiome assembly, suggesting that functional predictions will be aided by detailed information about the microbiome. At a longer timescale and lower-intensity disturbance (e.g., active layer deepening), deterministic processes likely dominate, making environmental parameters sufficient for predicting function. We propose that the contribution of stochastic and deterministic processes to post-thaw microbiome assembly depends on the characteristics of the thaw disturbance, as well as characteristics of the microbial community, such as the ecological and phylogenetic breadth of functional guilds, their functional redundancy, and biotic interactions. These propagate across space and time, potentially providing a means for predicting the microbial forcing of greenhouse gas feedbacks to global climate change.

Crop diversity promotes the recovery of fungal communities in saline-alkali areas of the Western Songnen Plain

“…Drift is the core of fungal community assembly ( Sheng et al, 2019 ). As plant diversity increases and input soil nutrients, the dominance of deterministic processes leads to a community well adapted to environmental conditions ( Ernakovich et al, 2022 ). These findings are supported by the results of the neutral model, which indicated that the mixture system led to higher environmental selection, indicating that a reduced degree of dispersal resulted from biological factors associated with increasing plant richness ( Supplementary Figure 5 ).…”

“…These findings are supported by the results of the neutral model, which indicated that the mixture system led to higher environmental selection, indicating that a reduced degree of dispersal resulted from biological factors associated with increasing plant richness ( Supplementary Figure 5 ). Conversely, stochastic processes increase the number of maladapted taxa and may reduce ecosystem function for some microbiomes ( Ernakovich et al, 2022 ). In addition, selection would lead to more similar phylogenetic groups and make their communities better aligned against external disturbances ( Yu et al, 2021 ).…”

Resistance, recovery, and resilience: rethinking the three Rs of survival in the Anthropocene

“…The terrestrial and subsea permafrost regions contain nearly 3,000 Gt of organic carbon, more than the sum of all other soil, the atmosphere, living biomass, and cumulative human emissions since the Industrial Revolution . These massive stocks of organic matter have been described as climate-protected, as they have been stabilized by persistent cold and wet conditions, which limit microbial and abiotic decomposition (Ernakovich et al 2022;. Gradual climate warming after the Last Glacial Maximum (LGM), some 26,500 years ago, resulted in over 100 meters of sea level rise, retreat of ice sheets, and widespread development of lakes and peatlands .…”

Climate change and emerging pathogens: Toward nature-based solutions

“…Equally as concerning is the observation that permafrost thaw releases ancient and novel pathogens entrapped as sub-zero microbiotome in permafrost ice for centuries [37,38] . Permafrost pathogens include parasites and fungi [39] , bacteria [40] , as well as DNA [41] , RNA [42] and giant viruses [43] . Taken together, the release of novel and ancient pathogens by melting permafrost poses timely and critical challenges to our immune system [44] , which is generally ill-equipped to confront new microbes, as the recent and ongoing pandemic confirms.…”