Permafrost thawing leads to the formation of thermokarst ponds that potentially emit CO2 and CH4 to the atmosphere. In the Nunavik subarctic region (northern Québec, Canada), these numerous, shallow ponds become well-stratified during summer. This creates a physico-chemical gradient of temperature and oxygen, with an upper oxic layer and a bottom low oxygen or anoxic layer. Our objective was to determine the influence of stratification and related limnological and landscape properties on the community structure of potentially active bacteria in these waters. Samples for RNA analysis were taken from ponds in three contrasting valleys across a gradient of permafrost degradation. A total of 1296 operational taxonomic units were identified by high throughput amplicon sequencing, targeting bacterial 16S rRNA that was reverse transcribed to cDNA. β-proteobacteria were the dominant group in all ponds, with highest representation by the genera Variovorax and Polynucleobacter. Methanotrophs were also among the most abundant sequences at most sites. They accounted for up to 27% of the total sequences (median of 4.9% for all samples), indicating the importance of methane as a bacterial energy source in these waters. Both oxygenic (cyanobacteria) and anoxygenic (Chlorobi) phototrophs were also well-represented, the latter in the low oxygen bottom waters. Ordination analyses showed that the communities clustered according to valley and depth, with significant effects attributed to dissolved oxygen, pH, dissolved organic carbon, and total suspended solids. These results indicate that the bacterial assemblages of permafrost thaw ponds are filtered by environmental gradients, and are complex consortia of functionally diverse taxa that likely affect the composition as well as magnitude of greenhouse gas emissions from these abundant waters.
Microbial diversity varies at multiple spatial scales, but little is known about how climate change may influence this variation. Here we assessed the free‐living bacterioplankton composition of thaw ponds over a north‐south gradient of permafrost degradation in the eastern Canadian subarctic. Three nested spatial scales were compared: 1) among ponds within individual valleys 2) between two valleys within each landscape type, and 3) between landscape types (southern sporadic versus northern discontinuous permafrost). As a reference point, we sampled rock‐basin lakes whose formation was not related to permafrost thawing. β‐diversity was low at the smallest scale despite marked differences in limnological properties among neighboring ponds. β‐diversity was high 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 that community assembly was driven by both stochastic (random extinction, dispersal, ecological drift) and deterministic (environmental filtering) processes. Communities sampled in the most degraded valley appeared primarily assembled through stochastic processes, while environmental filtering played a greater role at the other valleys. These results imply that climate warming and ongoing permafrost degradation will influence microbial community assembly, which in turn is likely to affect the functioning of thaw pond ecosystems.
Lakes and ponds derived from thawing permafrost are strong emitters of carbon dioxide and methane to the atmosphere, but little is known about the methane oxidation processes in these waters. Here we investigated the distribution and potential activity of aerobic methanotrophic bacteria in thaw ponds in two types of eroding permafrost landscapes in subarctic Québec: peatlands and mineral soils. We hypothesized that methanotrophic community composition and potential activity differ regionally as a function of the landscape type and permafrost degradation stage, and locally as a function of depth-dependent oxygen conditions. Our analysis of pmoA transcripts by Illumina amplicon sequencing and quantitative PCR showed that the communities were composed of diverse and potentially active lineages. Type I methanotrophs, particularly Methylobacter, dominated all communities, however there was a clear taxonomic separation between the two landscape types, consistent with environmental control of community structure. In contrast, methanotrophic potential activity, measured by pmoA transcript concentrations, did not vary with landscape type, but correlated with conductivity, phosphorus and total suspended solids. Methanotrophic potential activity was also detected in low-oxygen bottom waters, where it was inversely correlated with methane concentrations, suggesting methane depletion by methanotrophs. Methanotrophs were present and potentially active throughout the water column regardless of oxygen concentration, and may therefore be resilient to future mixing and oxygenation regimes in the warming subarctic.PLOS ONE | https://doi.org/10.1371/journal.pone
Abstract. Peatlands extend over vast areas of the northern landscape. Within some of these areas, lakes and ponds are changing in size as a result of permafrost thawing and erosion, resulting in mobilization of the carbon-rich peatland soils. Our aims in the present study were to characterize the particle, carbon and nutrient regime of a set of thermokarst (thaw) lakes and their adjacent peatland permafrost soils in a rapidly degrading landscape in subarctic Québec, Canada, and by way of fluorescence microscopy, flow cytometry, production measurements and an in situ enrichment experiment, determine the bacterial characteristics of these waters relative to other thaw lakes and rock-basin lakes in the region. The soil active layer in a degrading palsa (peatland permafrost mound) adjacent to one of the lakes contained an elevated carbon content (51 % of dry weight), high C : N ratios (17 : 1 by mass), and large stocks of other elements including N (3 % of dry weight), Fe (0.6 %), S (0.5 %), Ca (0.5 %) and P (0.05 %). Two permafrost cores were obtained to a depth of 2.77 m in the palsa, and computerized tomography scans of the cores confirmed that they contained high concentrations (> 80 %) of ice. Upon thawing, the cores released nitrate and dissolved organic carbon (from all core depths sampled), and soluble reactive phosphorus (from bottom depths), at concentrations well above those in the adjacent lake waters. The active layer soil showed a range of particle sizes with a peak at 229 µm, and this was similar to the distribution of particles in the upper permafrost cores. The particle spectrum for the lake water overlapped with those for the soil, but extended to larger (surface water) or finer (bottom water) particles. On average, more than 50 % of the bacterial cells and bacterial production was associated with particles > 3 µm. This relatively low contribution of free-living cells (operationally defined as the < 1 µm fraction) to bacterial production was a general feature of all of the northern lakes sampled, including other thaw lakes and shallow rock-basin lakes (average ± SE of 25 ± 6 %). However, a distinguishing feature of the peatland thaw lakes was significantly higher bacterial specific growth rates, which averaged 4 to 7 times higher values than in the other lake types. The in situ enrichment experiment showed no difference between organic carbon or phosphorus enrichment treatments at day 5 relative to the control, however there was an apparent increase in bacterial growth rates between days 1 and 5 in the soil and the carbon plus phosphorus enrichments. Collectively these results indicate that particles, nutrients and carbon are released by degrading permafrost peatland soils into their associated thermokarst lakes, creating favorable conditions for production by particle-based as well as free-living aquatic bacterial communities. The reduced bacterial concentrations despite high cellular growth rates imply that there is control of their population size by loss-related factors such as grazing and vira...
Abstract. Permafrost thaw lakes (thermokarst lakes) are widely distributed across the northern landscape, and are known to be biogeochemically active sites that emit large amounts of carbon to the atmosphere as CH4 and CO2. However, the abundance and composition of the photosynthetic communities that fix CO2 have been little explored in this ecosystem type. In order to identify the major groups of phototrophic organisms and their controlling variables, we sampled 12 permafrost thaw lakes along a permafrost degradation gradient in northern Québec, Canada. Additional samples were taken from five rock-basin reference lakes in the region to determine if the thaw lakes differed in limnological properties and phototrophs. Phytoplankton community structure was determined by high-performance liquid chromatography analysis of their photoprotective and photosynthetic pigments, and autotrophic picoplankton concentrations were assessed by flow cytometry. One of the black-colored lakes located in a landscape of rapidly degrading palsas (permafrost mounds) was selected for high-throughput 18S rRNA sequencing to complement conclusions based on the pigment and cytometry analyses. The results showed that the limnological properties of the thaw lakes differed significantly from the reference lakes, and were more highly stratified. However, both waterbody types contained similarly diverse phytoplankton groups, with dominance of the pigment assemblages by fucoxanthin-containing taxa, as well as chlorophytes, cryptophytes and cyanobacteria. Chlorophyll a concentrations (Chl a) were correlated with total phosphorus (TP), and both were significantly higher in the thaw lakes (overall means of 3.3 µg Chl a L−1 and 34 µg TP L−1) relative to the reference lakes (2.0 µg Chl a L−1 and 8.2 µg TP L−1). Stepwise multiple regression of Chl a against the other algal pigments showed that it was largely a function of alloxanthin, fucoxanthin and Chl b (R2 = 0.85). The bottom waters of two of the thaw lakes also contained high concentrations of bacteriochlorophyll d, showing the presence of green photosynthetic sulphur bacteria. The molecular analyses indicated a relatively minor contribution of diatoms, while chrysophytes, dinoflagellates and chlorophytes were well represented; the heterotrophic eukaryote fraction was dominated by numerous ciliate taxa, and also included Heliozoa, Rhizaria, chytrids and flagellates. Autotrophic picoplankton occurred in biovolume concentrations up to 3.1 × 105 µm3 picocyanobacteria mL−1 and 1.9 × 106 µm3 picoeukaryotes mL−1, with large variations among lakes. Both groups of picophytoplankton were positively correlated with total phytoplankton abundance, as measured by Chl a; picocyanobacteria were inversely correlated with dissolved organic carbon, while picoeukaryotes were inversely correlated with conductivity. Despite their net heterotrophic character, subarctic thaw lakes are rich habitats for diverse phototrophic communities.
Aerobic methanotrophic bacteria (methanotrophs) use methane as a source of carbon and energy, thereby mitigating net methane emissions from natural sources. Methanotrophs represent a widespread and phylogenetically complex guild, yet the biogeography of this functional group and the factors that explain the taxonomic structure of the methanotrophic assemblage are still poorly understood. Here, we used high‐throughput sequencing of the 16S rRNA gene of the bacterial community to study the methanotrophic community composition and the environmental factors that influence their distribution and relative abundance in a wide range of freshwater habitats, including lakes, streams and rivers across the boreal landscape. Within one region, soil and soil water samples were additionally taken from the surrounding watersheds in order to cover the full terrestrial–aquatic continuum. The composition of methanotrophic communities across the boreal landscape showed only a modest degree of regional differentiation but a strong structuring along the hydrologic continuum from soil to lake communities, regardless of regions. This pattern along the hydrologic continuum was mostly explained by a clear niche differentiation between type I and type II methanotrophs along environmental gradients in pH, and methane concentrations. Our results suggest very different roles of type I and type II methanotrophs within inland waters, the latter likely having a terrestrial source and reflecting passive transport and dilution along the aquatic networks, but this is an unresolved issue that requires further investigation.
The warming and thermal erosion of ice-containing permafrost results in thaw ponds that are strong emitters of methane to the atmosphere. Here we examined methanogens and other Archaea, in two types of thaw ponds that are formed by the collapse of either permafrost peat mounds (palsas) or mineral soil mounds (lithalsas) in subarctic Quebec, Canada. Using high-throughput sequencing of a hypervariable region of 16S rRNA, we determined the taxonomic structure and diversity of archaeal communities in near-bottom water samples, and analyzed the mcrA gene transcripts from two sites. The ponds at all sites were well stratified, with hypoxic or anoxic bottom waters. Their archaeal communities were dominated by Euryarchaeota, specifically taxa in the methanogenic orders Methanomicrobiales and Methanosarcinales, indicating a potentially active community of planktonic methanogens. The order Methanomicrobiales accounted for most of the mcrA transcripts in the two ponds. The Archaeal communities differed significantly between the lithalsa and palsa ponds, with higher alpha diversity in the organic-rich palsa ponds, and pronounced differences in community structure. These results indicate the widespread occurrence of planktonic, methane-producing Archaea in thaw ponds, with environmental selection of taxa according to permafrost landscape type.
Abstract. Permafrost thaw ponds and lakes are widespread across the northern landscape and may play a central role in global biogeochemical cycles, yet knowledge about their microbial ecology is limited. We sampled a set of thaw ponds and lakes as well as shallow rock-basin lakes that are located in distinct valleys along a North–South permafrost degradation gradient. We applied high-throughput sequencing of the 16S rRNA gene to determine co-occurrence patterns among bacterial taxa, and then analyzed these results relative to environmental variables to identify factors controlling bacterial community structure. Network analysis was applied to identify possible ecological linkages among the bacterial taxa and with abiotic and biotic variables. The results showed an overall high level of shared taxa among bacterial communities within each valley, however the bacterial co-occurrence patterns were non-random, with evidence of habitat preferences. There were taxonomic differences in bacterial assemblages among the different valleys that were statistically related to dissolved organic carbon concentration, conductivity and phytoplankton biomass. Co-occurrence networks revealed complex interdependencies within the bacterioplankton communities and showed contrasting linkages to environmental conditions among the main bacterial phyla. The thaw pond networks were composed of a limited number of highly connected taxa. This "small world network" property would render the communities more robust to environmental change but vulnerable to the loss of microbial keystone species.
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