Microbiome assembly in thawing permafrost and its feedbacks to climate

• Published in: Global change biology Vol. 28; no. 17; pp. 5007 - 5026
• Main Authors: Ernakovich, Jessica G., Barbato, Robyn A., Rich, Virginia I., Schädel, Christina, Hewitt, Rebecca E., Doherty, Stacey J., Whalen, Emily D., Abbott, Benjamin W., Barta, Jiri, Biasi, Christina, Chabot, Chris L., Hultman, Jenni, Knoblauch, Christian, Vetter, Maggie C. Y. Lau, Leewis, Mary‐Cathrine, Liebner, Susanne, Mackelprang, Rachel, Onstott, Tullis C., Richter, Andreas, Schütte, Ursel M. E., Siljanen, Henri M. P., Taş, Neslihan, Timling, Ina, Vishnivetskaya, Tatiana A., Waldrop, Mark P., Winkel, Matthias
• Format: Journal Article
• Language: English
• Published: Oxford Blackwell Publishing Ltd 01.09.2022; Wiley-Blackwell
• Subjects: Assembly; Biogeochemistry; Climate change; Community structure; Environmental changes; Environmental conditions; Environmental factors; ENVIRONMENTAL SCIENCES; Greenhouse gases; Guilds; Metabolism; Microbial activity; Microbiology; Microbiomes; Microorganisms; Organic matter; Permafrost; Phylogeny; Polar environments; Redundancy; Stochastic processes; Stochasticity; Thawing; Time
• ISSN: 1354-1013; 1365-2486
• DOI: 10.1111/gcb.16231

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. Microbial communities are active players in climate feedbacks from permafrost thaw. Ecological assembly shapes post‐thaw microbial community composition through deterministic and stochastic processes. In intact permafrost, communities are shaped by selection for permafrost conditions and dispersal limitation. In early thaw, assembly is dominated by dispersal of new members (yellow and orange arrows) and drift (red x’s). Over time, the cumulative impact of selection by abiotic and biotic post‐thaw conditions increases (depicted by filters), and genetic diversification occurs (shown by changes in organism color). Functional guild composition of newly assembled communities impacts post‐thaw ecosystem processes. Artwork by Victor O. Leshyk.