Microbial biogeography of permafrost thaw ponds

Permafrost thaw ponds are increasing in size and numbers in northern Quebec landscape (Sheldrake River valley; 56°36.66′N, 76°12.93′W). The extent and stage of thawing of the surrounding permafrost determine the spatial distribution as well as the main limnological characteristics of these water bodies over multiple scales, which make them suitable systems to investigate microbial biogeography. Photo: Jérôme Comte.

EDITOR'S CHOICE JULY

By Jérôme Comte

Microorganisms are reported to display biogeographic patterns across a broad range of spatial scales but the processes that create and maintain such patterns are not well understood. Community β-diversity is shaped by the interplay between deterministic non-random, niche-based mechanisms, and random neutral processes. Currently, there is an intense debate whether microbial biogeography is determined exclusively by local contemporary environmental conditions, or whether dispersal barriers exist. Less studied is how climate change may influence the spatial variation in microbial diversity. Climate change is causing large-scale transformations of high latitude landscapes including the northward retreat of the permafrost boundary and the expansion of permafrost thaw ponds.

Permafrost thaw ponds have the potential to mobilize large quantities of organic carbon that were previously stored in the frozen tundra soils. These waters have not been considered in global greenhouse gas budgets because of their small size, but they may be collectively important given their occurrence in large numbers throughout the circumpolar region. In the subarctic region of Quebec (Nunavik), these water bodies are increasing in size and abundance but little is known about the biodiversity they host. Permafrost thaw ponds present a great variability in their limnological characteristics including striking differences in their optical properties due to varied combinations of dissolved organic matter and suspended particles. The extent and stage of thawing of the surrounding permafrost influence the landscape characteristics (e.g. vegetation cover, landscape area covered by aquatic systems) and the geomorphology of the ponds creating a gradient in concentrations of allochthonous dissolved organic matter (DOM), which may shape microbial communities and in turn the functioning of permafrost thaw ponds. Our project aimed to investigate the spatial structure of natural microbial communities as well as the influence of climate related changes on community assembly mechanisms.

We determined the microbial composition of thaw ponds over a North-South gradient of permafrost degradation in the eastern Canadian subarctic. Three nested spatial scales were compared: (i) among ponds within individual valleys (ii) between two valleys within each permafrost landscape type, and (iii) between two landscape types (southern highly degraded versus northern discontinuous permafrost). As a reference point, we sampled rock-basin lakes whose formation was not related to permafrost thawing.

There was little β-diversity at the smallest scale despite marked differences in limnological properties among neighboring ponds. Greater β-diversity was detected among valleys, associated with greater environmental heterogeneity. The largest differences were between landscape types and appeared to reflect the concomitant effects of environmental filtering and dispersal limitation. Raup-Crick β-diversity indicated pronounced differences in community assembly processes along the permafrost gradient, with high stochasticity leading to high similarity between the northern valleys and deterministic processes explaining differences between the southern valleys.

This study showed that thaw ponds are diverse and that the composition of these complex microbial consortia is mainly shaped by environmental filtering. In addition, this work implies that microbial community assembly, which in turn is likely to affect ecosystem functioning, may be influenced by climate warming and degradation of permafrost landscapes.

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