Permafrost microbial communities and functional genes are structured by latitudinal and soil geochemical gradients

Abstract

Permafrost underlies approximately one quarter of Northern Hemisphere terrestrial surfaces and contains 25-50% of the global soil carbon (C) pool. Permafrost soils and the C stocks within are vulnerable to ongoing and future projected climate warming. The biogeography of microbial communities inhabiting permafrost has not been examined beyond a small number of sites focused on local-scale variation. Permafrost is different from other soils. Perennially frozen conditions in permafrost dictate that microbial communities do not turn over quickly, thus possibly providing strong linkages to past environments. Thus, the factors structuring the composition and function of microbial communities may differ from patterns observed in other terrestrial environments. Here, we analyzed 133 permafrost metagenomes from North America, Europe, and Asia. Permafrost biodiversity and taxonomic distribution varied in relation to pH, latitude and soil depth. The distribution of genes differed by latitude, soil depth, age, and pH. Genes that were the most highly variable across all sites were associated with energy metabolism and C-assimilation. Specifically, methanogenesis, fermentation, nitrate reduction, and replenishment of citric acid cycle intermediates. This suggests that adaptations to energy acquisition and substrate availability are among some of the strongest selective pressures shaping permafrost microbial communities. The spatial variation in metabolic potential has primed communities for specific biogeochemical processes as soils thaw due to climate change, which could cause regional- to global- scale variation in C and nitrogen processing and greenhouse gas emissions.

Fig. 1. Geographic distribution of sampling locations and taxonomic composition of microbial communities in permafrost.

A Permafrost sample locations overlayed onto a map showing mean annual ground temperature (MAGT) [46]. Map used with permission. B Relative abundance of bacterial and archaeal phyla across permafrost samples. C Unimodal relationship between Shannon diversity and permafrost pH. Different colors/shapes represent different locations. R² = 0.06, p = 0.019. Shannon diversity at the class level = 2.945 - 0.116*pH - 0.0668*(pH-6.933)². With Vault Creek Tunnel outlier samples excluded R² = 0.14, p < 0.0001.

Fig. 2. Six primary sample clusters vary by pH, latitude, and soil depth.

Average pH for each cluster is shown on the x-axis and average latitude for each cluster is shown on the y-axis. Relative soil depth is indicated by circle size, in which larger size indicates greater depths.

Fig. 3. Heatmap and pathway diagrams of the most highly variable KEGG genes occurring across permafrost sites.

Heatmap shows the scaled relative abundances of KEGG genes that were the most variable across sites, which were clustered using Ward’s minimum variance method. Genes clustered into two primary groups, A and B, which are shown with cool and warm colors, respectively. Subgroups within A are colored dark purple (A1) and green (A2). Subgroups within B are colored orange (B1) and red (B2). Samples (shown in rows) are those occurring in the six primary sample clusters and are organized by cluster for the purpose of visualization. They are labeled by cluster number and a description (including latitude, pH, depth, and archaeal abundance). Clusters 5 and 6 have a similar latitude and pH, and so are labeled by the relative abundance of archaeal genes (archaea-enriched versus non-archaeal) to differentiate between them. Colored boxes overlaid on the heatmap highlight the relationships between groups of genes and clusters of sites. Pathways from each gene group are shown next to the heatmap and are colored dark purple, green, orange, or red to indicate which group they belong to (A1, A2, B1, B2, respectively). Genes from the Ethylmalonyl Co-A pathway were found in Groups B1 and B2, which is indicated by dual coloring of the pathway with red and orange. KO numbers are followed by either a gene name or description in parentheses. The full list of highly variable genes with complete descriptions (shown in the order in which they occur in the heatmap) is available in ScienceBase. In pathway diagrams, dashed arrows indicate multiple steps that are not shown. For the glyoxylate pathway diagram, the abbreviations are as follows: glyoxylate (GLY), malate (MAL), oxaloacetate (OAA), citrate (CIT), isocitrate (ISO), and succinate (SUC).

Fig. 4. Proposed model of permafrost microbial community assembly.

Paleoenvironmental factors, such as plant community structure, climate, mechanism of permafrost formation, and water regimes shape soil microbial communities. Paleoenvironment also establishes soil physicochemical conditions within permafrost that, in combination with static subzero conditions, act through time to shape modern communities. Filter size reflects time since permafrost formation and filter color indicates differing environmental conditions. Immigration into permafrost is limited because subzero temperatures restrict water flow, so contemporary microorganisms are largely a subset of past communities that have undergone environmental filtering and diversification. Figure created in Adobe Illustrator and Biorender.