Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake

Vigneron, Adrien; Lovejoy, Connie; Cruaud, Perrine; Kalenitchenko, Dimitri; Culley, Alexander I.; Vincent, Warwick F.

doi:10.3389/fmicb.2019.01656

Cited by 52 publications

(79 citation statements)

References 68 publications

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“…Previous studies that have explored the seasonal patterns in methanotrophic communities have reported dominance of type I methanotrophs during cold seasons (Ricão Canelhas, Denfeld, Weyhenmeyer, Bastviken, & Bertilsson, 2016;Samad & Bertilsson, 2017;Vigneron et al, 2019). However, we only found a significant and unimodal relationship between type II methanotrophs relative abundance and temperature, perhaps due to fact that most of the samples were taken during the summer and the temperature gradient was relatively modest.…”

Section: Niche Differentiation Between Type I and Type Ii Methanotrcontrasting

confidence: 82%

“…Temperature has been shown to play a major role in regulating aquatic methane dynamics (Börjesson, Sundh, & Svensson, ; Graef, Hestnes, Svenning, & Frenzel, ; He et al, ; Mohanty, Bodelier, & Conrad, ; Wagner, Lipski, Embacher, & Gattinger, ; Wartiainen et al, ), and our results support these findings. Previous studies that have explored the seasonal patterns in methanotrophic communities have reported dominance of type I methanotrophs during cold seasons (Ricão Canelhas, Denfeld, Weyhenmeyer, Bastviken, & Bertilsson, ; Samad & Bertilsson, ; Vigneron et al, ). However, we only found a significant and unimodal relationship between type II methanotrophs relative abundance and temperature, perhaps due to fact that most of the samples were taken during the summer and the temperature gradient was relatively modest.…”

Section: Discussionmentioning

confidence: 97%

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Large‐scale biogeography and environmental regulation of methanotrophic bacteria across boreal inland waters

et al. 2019

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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.

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Section: Niche Differentiation Between Type I and Type Ii Methanotrcontrasting

confidence: 82%

Section: Discussionmentioning

confidence: 97%

Large‐scale biogeography and environmental regulation of methanotrophic bacteria across boreal inland waters

et al. 2019

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“…However, this was less than the corresponding amount of CO 2 accumulated in summer, which on average was about 30% greater, resulting in a much higher ratio of diffusive CO 2 to CH 4 flux in summer. This may be an indication of the predominance of hydrogenotrophy and use of CO 2 for methanogenesis in these fully anoxic environments during the winter ice cover period (consistent with metagenomic observations of abundant hydrogenotrophic Methanomicrobiales in these waters in winter; Vigneron et al, 2019), followed by increased respiration by aerobic bacteria in summer accompanied by the methanotrophic oxidation of CH 4 (Crevecoeur et al, 2015). In addition, the lake ice stored both CH 4 and CO 2 , in quantities of up to 5% of the water column quantities.…”

Section: Journal Of Geophysical Research: Biogeosciencessupporting

confidence: 82%

Winter Accumulation of Methane and its Variable Timing of Release from Thermokarst Lakes in Subarctic Peatlands

2019

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Previous studies of thermokarst lakes have drawn attention to the potential for accumulation of CH 4 under the ice and its subsequent release in spring; however, such observations have not been available for thermokarst waters in carbon-rich peatlands. Here we undertook a winter profiling of five black-water lakes located on eroding permafrost peatlands in subarctic Quebec for comparison with summer profiles and used a 2-year data set of automated water temperature, conductivity, and oxygen measurements to evaluate how the annual mixing dynamics may affect the venting of greenhouse gases to the atmosphere. All of the sampled lakes contained large amounts of dissolved CH 4 under their winter ice cover. These sub-ice concentrations were up to 5 orders of magnitude above air equilibrium (i.e., the expected concentration in lake water equilibrated with the atmosphere), resulting in calculated emission rates at ice breakup that would be 1-2 orders of magnitude higher than midsummer averages. The amount of CO 2 dissolved in the water column was reduced in winter, and the estimated ratio of potential diffusive CO 2 to CH 4 emission in spring was half the measured summer ratio, suggesting a seasonal shift in methanogenesis and bacterial activity. All surface lake ice contained bubbles of CH 4 and CO 2 , but this amounted to <5% of the total amount of the dissolved CH 4 and CO 2 in the corresponding lake water column. The continuous logging records suggested that lake morphometry may play a role in controlling the timing and extent of CH 4 and CO 2 release from the water column to the atmosphere.Plain Language Summary Waterbodies that are formed by the thawing and collapse of ice-rich permafrost ("thermokarst lakes") are known to be major sources of greenhouse emissions in northern landscapes, but the seasonal variation in these emissions is not well understood. In this study, we measured the concentrations of methane and carbon dioxide beneath the ice of five thermokarst lakes in late winter and compared these with summer concentrations and profiles. These "black-water lakes" are located in subarctic peatlands and are darkly colored because of their high concentrations of permafrost-derived, colored organic carbon. The results showed a winter accumulation of gases beneath the ice that would result in 10 to 100 times greater emissions from the surface waters at spring ice breakup than during summer open water conditions. However, continuous in situ measurements of water temperature and oxygen showed that lakes with smaller area to depth ratios may partially retain greenhouse gases that accumulated in their bottom waters throughout winter, thereby limiting the loss of methane in spring that would otherwise occur. More complete mixing occurred during fall cooling and circulation, and release of gases accumulated in the bottom waters during winter and summer may occur at that time. The exact volume of lake water that is mixed during the spring and fall periods is likely related to the wind fetch and depth of the basin. These...

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“…1). The microbial community of the oxic mixolimnion beneath the ice was consistent with cold freshwater communities, with lineages of the Verrucomicrobia, Bacteroidetes, Actinobacteria, Cyanobacteria and Betaproteobacteria, which are frequently observed in lakes and rivers [25][26][27]. At the chemocline, alphaproteobacterial chemotrophic sulfur oxidizers and phototrophic sulfur oxidizers (Chlorobiaceae), both previously observed in microbial surveys of Antarctica [17,28] and temperate meromictic lakes [19,29] co-occurred since the lower depth limits of the Lake A photic and aerobic zones coincided (Fig.…”

Section: Discussionmentioning

confidence: 68%

Sulfur intermediates as new biogeochemical hubs in an aquatic model microbial ecosystem

Vigneron

Cruaud

Culley

et al. 2020

Preprint

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BackgroundThe sulfur cycle encompasses a series of complex aerobic and anaerobic transformations of S-containing molecules, and plays a fundamental role in cellular and ecosystems level-processes, influencing biological carbon transfers and other biogeochemical cycles. Despite their importance, the microbial communities and metabolic pathways involved in these transformations remain poorly understood, notably for inorganic sulfur compounds of intermediate oxidation states (thiosulfate, tetrathionate, sulfite, polysulfides). Isolated and highly stratified, the extreme geochemical and environmental contexts of the meromictic ice-capped Lake A, in the Canadian High Arctic, provides an outstanding model ecosystem to resolve the distribution and metabolism of aquatic sulfur cycling microorganisms along redox and salinity gradients. ResultsApplying complementary molecular approaches, we identified sharply contrasting microbial communities and metabolic potentials among the distinct water layers of the Lake A, with homologies to diverse fresh, brackish and saline water microbiomes. Sulfur cycling genes were abundant at all depths, with oxidative processes in the oxic freshwater layers, reductive reactions in the anoxic and sulfidic bottom waters and genes for both transformations at the chemocline, and co-varied with bacterial abundance. Up to 154 different genomic bins with potential for sulfur transformation were recovered, revealing a panoply of taxonomically diverse microorganisms with complex metabolic pathways for biogeochemical sulfur reactions. Metabolism of sulfur cycle intermediates was widespread throughout the water column, co-occurring with sulfate reduction or sulfide oxidation pathways. The genomic bin composition suggested that in addition to chemical oxidation, these intermediate sulfur compounds were likely produced by the predominant sulfur chemo- and photo-oxidizers at the chemocline and by diverse microbial organic sulfur molecule degraders. ConclusionsThe Lake A microbial ecosystem provided an ideal opportunity to identify new features of the biogeochemical sulfur cycle. Our detailed metagenomic analyses across the broad physico-chemical gradients of this highly stratified lake extend the known diversity of microorganisms and metabolic pathways involved in sulfur transformations over a wide range of environmental conditions. The results identify the importance of sulfur cycle intermediates and organic sulfur molecules as major sources of electron donors and acceptors for aquatic and sedimentary microbial communities in association with the classical sulfur cycle.

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Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake

Cited by 52 publications

References 68 publications

Large‐scale biogeography and environmental regulation of methanotrophic bacteria across boreal inland waters

Large‐scale biogeography and environmental regulation of methanotrophic bacteria across boreal inland waters

Winter Accumulation of Methane and its Variable Timing of Release from Thermokarst Lakes in Subarctic Peatlands

Sulfur intermediates as new biogeochemical hubs in an aquatic model microbial ecosystem

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