4.8 Article

Microbiome assembly in thawing permafrost and its feedbacks to climate

Journal

GLOBAL CHANGE BIOLOGY
Volume 28, Issue 17, Pages 5007-5026

Publisher

WILEY
DOI: 10.1111/gcb.16231

Keywords

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Funding

  1. Academy of Finland [290315, 313114, 314630]
  2. EU [773421]
  3. Germany's Excellence Strategy [EXC 2037]
  4. Grantova Agentura Ceske Republiky [20-21259J]
  5. National Aeronautics and Space Administration [NNH15AB58I, NNX15AM12G]
  6. New Hampshire Agriculture Experiment Station
  7. U.S. Army Basic and Applied Research Program
  8. U.S. Department of Energy [DE-SC0020369]
  9. U.S. Geological Survey
  10. United States Department of Energy Office of Biological and Environmental Research [DE-SC0016440]
  11. United States National Science Foundation [1331083, 1916565, 1931333, 2022070, DEB-1442262]
  12. National Science Foundation [2144961]
  13. U.S. Department of Energy (DOE) [DE-SC0020369, DE-SC0016440] Funding Source: U.S. Department of Energy (DOE)
  14. Academy of Finland (AKA) [290315, 314630, 314630, 290315] Funding Source: Academy of Finland (AKA)

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The physical and chemical changes that occur during permafrost thaw have a direct impact on microbial communities, which in turn affect biogeochemistry and climate feedbacks. The proposed Assembly Theory framework provides a way to understand the changes in microbial communities and their implications for community function and climate feedbacks.
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.

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