Influence du dégel du pergélisol sur la matière organique et les réseaux trophiques dans les eaux douces circumpolaires nordiques

Les sols gelés en permanence du paysage circumpolaire constituent l’un des plus grands gisements de carbone organique sur Terre. Le réchauffement climatique et le dégel du pergélisol qu’il entraîne ont accru le risque qu'une grande partie de ce carbone soit libérée dans l'atmosphère sous forme de gaz à effet de serre, notamment sous forme de méthane depuis les nombreux écosystèmes aquatiques présents dans les régions subarctiques et arctiques. Ce scénario a attiré l'attention de la communauté scientifique sur le cycle du carbone dans les écosystèmes circumpolaires. Cependant, les changements induits par ces apports croissants de matière terrestre sur le réservoir de carbone organique et sur le réseau alimentaire des lacs et des étangs nordiques ont été peu étudiés. Ce projet de thèse vise à explorer l'influence du dégel du pergélisol sur les lacs de haute latitude. Premièrement, nous avons évalué les effets du dégel du pergélisol sur la matière organique dissoute (MOD) par des analyses optiques de 253 étangs couvrant 200 degrés de longitude à travers l’Arctique. Pour un sous-échantillon de dix plans d’eau subarctiques, nous avons également quantifié la contribution terrestre à la MOD en utilisant l’approche des isotopes stables. Dans un second temps, en mesurant la concentration en nutriments et en chlorophylle a, et en utilisant des approches basées sur les acides gras et les isotopes stables, nous avons étudié l’influence du dégel du pergélisol sur les producteurs et les consommateurs primaires de la chaîne alimentaire planctonique au sein de huit étangs subarctiques impactés différemment par les apports terrestres venant du bassin versant. Enfin, nous avons exploré la communauté et la biomasse de zooplancton dans huit étangs de dégel subarctiques, ainsi que la manière avec laquelle la stratification thermique et les variables environnementales associées déterminent la distribution verticale du zooplancton dans ces mares arctiques fortement affectées par le dégel du pergélisol. Les mesures optiques montrent une plus forte proportion de carbone terrestre et une moindre contribution des algues à la MOD dans les eaux touchées par le dégel du pergélisol. La composition de la MOD est largement dominée (moyenne de 93%) par de la matière d’origine terrestre dans les sites influencés par le dégel du pergélisol, tandis que l'influence terrestre est beaucoup moins importante dans les masses d'eau situées dans des bassins hydrographiques non affectés par des processus thermokarstiques (39%). De plus, nos résultats mettent en évidence l’influence positive du dégel du pergélisol sur la teneur en nutriments et l’abondance en algues planctoniques. Cependant, l'impact sur les consommateurs primaires reste très limité, avec une faible contribution de la matière organique terrestre à la biomasse du zooplancton dans les étangs de dégel subarctiques (35% selon l’approche basée sur les isotopes stables, 18% selon celle basée sur les acides gras). Enfin, cette thèse fait état de la prédominance des rotifères dans les mares de thermokarst subarctiques (35 à 93% de la biomasse du zooplancton) et met en évidence la stratification prononcée du zooplancton, laquelle est principalement déterminée par un compris entre l’accès à suffisamment d’oxygène (O2) et à une diète algale de qualité, ainsi qu’à la pression de prédation exercée par des larves de Chaoborus. Pris collectivement, ces résultats soulignent la forte influence du dégel du pergélisol sur le réservoir de carbone organique des eaux douces septentrionales, avec une tendance à la domination croissante du carbone organique d'origine terrestre pouvant altérer les voies métaboliques et les processus biogéochimiques dans le Nord. Ces impacts peuvent être considérés comme un exemple extrême de brunissement qui va probablement altérer les lacs de haute latitude vers des conditions davantage hétérotrophiques et alimenter leur boucle microbienne. En outre, alors que le dégel du pergélisol stimule la croissance du phytoplancton aux dépens des algues benthiques, ces mêmes producteurs primaires planctoniques semblent être la principale ressource qui supporte le réseau alimentaire dans les étangs de dégel, indépendamment de l’écrasante domination de la matière organique issue du bassin versant. Enfin, le réchauffement et le brunissement à venir des plans d’eau circumpolaires devraient renforcer la stabilité thermique des lacs, augmentant ainsi le risque d'anoxie dans la colonne d'eau, et créant par conséquent une incertitude quant à la réponse future de la communauté zooplanctonique face au réchauffement climatique et au dégel du pergélisol. Frozen tundra soils are one of the largest pools of organic carbon in the Earth system. Climate warming and the associated permafrost thaw have increased the risk that a large fraction of this carbon will be released to the atmosphere as greenhouse gases, particularly in the form of methane produced by the numerous aquatic ecosystems found throughout the subarctic and arctic regions. This scenario has drawn the attention of the scientific community to the carbon cycle in circumpolar ecosystems. Some of this carbon released from thawing permafrost is transported into freshwater systems. However, the changes to the carbon pool and the northern freshwater food webs by the increased terrigenous input have not been studied extensively. This PhD project aims to investigate how permafrost thaw influences northern waterbodies across the Arctic. First, we evaluated the effects of thawing ice-rich permafrost on the dissolved organic matter (DOM) in freshwaters. We used optical analyses of 253 ponds covering 200 degrees of longitude across the circumpolar North. For a subset of 10 waterbodies in subarctic Quebec, we used stable isotopes (SI) to quantify the contribution of terrestrial sources to the DOM pool. Second, using nutrients, chlorophyll a, fatty acids (FA), and SI, we investigated the influence of thawing permafrost on primary producers and primary consumers of the planktonic food web of 8 subarctic ponds affected to different degrees by permafrost carbon. Finally, we explored the zooplankton community and biomass in 8 subarctic thaw ponds and determined the extent to which thermal stratification and the associated environmental variables drive the vertical distribution of zooplankton in these arctic freshwaters that are affected by degrading ice-rich permafrost. The optical measurements reveal a higher proportion of terrestrial carbon and a lower algal contribution to DOM in waters affected by thawing permafrost. DOM composition is dominated largely (mean of 93%) by terrestrial substances at sites influenced by thawing permafrost, whereas the terrestrial influence is much less (39%) in waterbodies located in catchments unaffected by thermokarst processes. Also, our results highlight the stimulating influence of eroding and degrading ice-rich permafrost on nutrients and planktonic algae. However, the effect on consumers remains relatively constrained, with a limited contribution of terrestrial organic matter to the biomass of the filter-feeding zooplankton in subarctic thaw ponds (35% according to SI- and 18% according to FA-based mixing models). Finally, this thesis reports the dominance of rotifers in subarctic thaw ponds (35–93% of the zooplankton biomass), and highlights the pronounced stratification of zooplankton that is driven mostly by a combination of oxygen (O2), Chaoborus predation, phytoplankton, and essential FA supply. Collectively, these findings emphasize the strong influence of thawing permafrost on the carbon pool of northern freshwaters and a shift toward increased dominance by land-derived organic carbon that may alter metabolic pathways and biogeochemical processes in the North. These impacts may be considered as an extreme example of browning that will likely shift high-latitude freshwaters more toward net heterotrophic conditions and fuel the microbial loop. Furthermore, while permafrost thaw stimulates phytoplankton growing in the water column at the expense of benthic algae, these same planktonic primary producers appear to be the key resource that fuels the food web in thaw ponds, regardless of the overwhelming dominance of terrigenous organic matter. Finally, future warming and browning of circumpolar freshwaters are expected to enhance the thermal stability of thaw ponds. This will increase the risk of anoxia throughout the water column and, as such, add uncertainty as to the future response of arctic and subarctic zooplankton communities to global warming and degrading permafrost

Hidden stores of organic matter in northern lake ice : Selective retention of terrestrial particles, phytoplankton and labile carbon

Around 50% of the world's lakes freeze seasonally, but the duration of ice-cover is shortening each year and this is likely to have broad limnological consequences. We sampled freshwater ice and the underlying water in 19 boreal and polar lakes to evaluate whether lake ice contains an inoculum of algae, nutrients, and carbon that may contribute to lake ecosystem productivity. Boreal and Arctic lakes differed in ice duration (6 vs. >10 months), thickness (70 vs. 190 cm), and quality (predominantly snow ice vs. black ice), but in all lakes, there were consistent differences in biological and biogeochemical composition between ice and water. Particulate fractions were often more retained while most dissolved compounds were excluded from the ice; for example, the ice had more terrestrial particulate carbon, measured as fatty acid biomarkers (averages of 1.1 vs. 0.3 µg L−1) but lower dissolved organic carbon (2.2 vs. 5.7 mg C L−1) and inorganic phosphorus concentrations (4.0 vs. 7.5 µg C L−1) than the underlying water. The boreal ice further had three times higher chlorophyll-a, than the water (0.9 vs. 0.3 µg L−1). Of the dissolved fractions, the contribution of protein-like compounds was higher in the ice, and this in all lakes. These labile compounds would become available to planktonic microbes when the ice melts. Our results show that freshwater ice has an underestimated role in storage and transformation in the biogeochemical carbon cycle of ice-covered lake ecosystems

Declining fungal diversity in Arctic freshwaters along a permafrost thaw gradient

Climate change-driven permafrost thaw has a strong influence on pan-Arctic regions, via, for example, the formation of thermokarst ponds. These ponds are hotspots of microbial carbon cycling and greenhouse gas production, and efforts have been put on disentangling the role of bacteria and archaea in recycling the increasing amounts of carbon arriving to the ponds from degrading watersheds. However, despite the well-established role of fungi in carbon cycling in the terrestrial environments, the interactions between permafrost thaw and fungal communities in Arctic freshwaters have remained unknown. We integrated data from 60 ponds in Arctic hydro-ecosystems, representing a gradient of permafrost integrity and spanning over five regions, namely Alaska, Greenland, Canada, Sweden, and Western Siberia. The results revealed that differences in pH and organic matter quality and availability were linked to distinct fungal community compositions and that a large fraction of the community represented unknown fungal phyla. Results display a 16%-19% decrease in fungal diversity, assessed by beta diversity, across ponds in landscapes with more degraded permafrost. At the same time, sites with similar carbon quality shared more species, aligning a shift in species composition with the quality and availability of terrestrial dissolved organic matter. We demonstrate that the degradation of permafrost has a strong negative impact on aquatic fungal diversity, likely via interactions with the carbon pool released from ancient deposits. This is expected to have implications for carbon cycling and climate feedback loops in the rapidly warming Arctic

Ontogenic succession of thermokarst thaw ponds is linked to dissolved organic matter quality and microbial degradation potential

Warming climate is thawing the permafrost in arctic and subarctic regions, leading to formation of thermokarst ponds. During the formation and geomorphological succession of these ponds, carbon that has been trapped in frozen soils for thousands of years is hydrologically mobilized and returned to the active carbon cycle. We sampled 12 thermokarst ponds representing three different stages of pond succession to study the potential of microbial communities to metabolize the organic carbon in the water. We investigated the quality of the dissolved organic carbon (DOC) in the water column based on the spectrophotometric and fluorometric properties of the chromophoric dissolved organic matter combined with parallel factor analysis and the potential of the microbial community for degrading these carbon compounds based on genetic markers related to carbon degradation. Our analysis showed a clear difference in the DOC quality across the different developmental stages. In the younger ponds, organic matter quality suggested that it was originating from the degrading permafrost and in the metagenomes collected from these ponds, the normalized abundance of genes related to degradation of carbon compounds was higher. There was also a shift in the degradation potential in the water column of the ponds, with higher potential for organic matter degradation in deeper, anoxic layers. In conclusion, our results show that the DOC quality and the genetic potential of the microbial community for carbon cycling change across the pond ontogeny, suggesting a capacity of the microbial communities to adapt to changing environmental conditions

Community composition of aquatic fungi across the thawing Arctic

Thermokarst activity at permafrost sites releases considerable amounts of ancient carbon to the atmosphere. A large part of this carbon is released via thermokarst ponds, and fungi could be an important organismal group enabling its recycling. However, our knowledge about aquatic fungi in thermokarstic systems is extremely limited. In this study, we collected samples from five permafrost sites distributed across circumpolar Arctic and representing different stages of permafrost integrity. Surface water samples were taken from the ponds and, additionally, for most of the ponds also the detritus and sediment samples were taken. All the samples were extracted for total DNA, which was then amplified for the fungal ITS2 region of the ribosomal genes. These amplicons were sequenced using PacBio technology. Water samples were also collected to analyze the chemical conditions in the ponds, including nutrient status and the quality and quantity of dissolved organic carbon. This dataset gives a unique overview of the impact of the thawing permafrost on fungal communities and their potential role on carbon recycling

Declining fungal diversity in Arctic freshwaters along a permafrost thaw gradient

Climate change-driven permafrost thaw has a strong influence on pan-Arctic regions, via, for example, the formation of thermokarst ponds. These ponds are hotspots of microbial carbon cycling and greenhouse gas production, and efforts have been put on disentangling the role of bacteria and archaea in recycling the increasing amounts of carbon arriving to the ponds from degrading watersheds. However, despite the well-established role of fungi in carbon cycling in the terrestrial environments, the interactions between permafrost thaw and fungal communities in Arctic freshwaters have remained unknown. We integrated data from 60 ponds in Arctic hydro-ecosystems, representing a gradient of permafrost integrity and spanning over five regions, namely Alaska, Greenland, Canada, Sweden, and Western Siberia. The results revealed that differences in pH and organic matter quality and availability were linked to distinct fungal community compositions and that a large fraction of the community represented unknown fungal phyla. Results display a 16%-19% decrease in fungal diversity, assessed by beta diversity, across ponds in landscapes with more degraded permafrost. At the same time, sites with similar carbon quality shared more species, aligning a shift in species composition with the quality and availability of terrestrial dissolved organic matter. We demonstrate that the degradation of permafrost has a strong negative impact on aquatic fungal diversity, likely via interactions with the carbon pool released from ancient deposits. This is expected to have implications for carbon cycling and climate feedback loops in the rapidly warming Arctic

Biogeochemical Distinctiveness of Peatland Ponds, Thermokarst Waterbodies, and Lakes

Small lentic freshwater ecosystems play a disproportionate role in global biogeochemical cycles by processing large amounts of carbon (C), nitrogen (N), and phosphorus (P), but it is unlikely that they behave as one homogenous group for the purpose of extrapolation. Here, we synthesize biogeochemical data from >12,000 geographically distinct freshwater systems: lakes, peatland ponds, and thermokarst waterbodies. We show that peatland ponds are biogeochemically distinct from the more widely studied lake systems, while thermokarst waterbodies share characteristics with peatland ponds, lakes, or both. For any given size or depth, peatland ponds tend to have dissolved organic carbon concentrations several-fold higher and are 100-fold more acidic than lakes because of the organic matter-rich settings in which they develop. The biogeochemical distinctiveness of freshwater ecosystems highlights the need to account for the fundamental differences in sources and processing of organic matter to understand and predict their role in global biogeochemical cycles