Implications of a changing Arctic on microbial communities: Following the effects of thawing permafrost from land to sea

Abstract

Climate change has severe impacts in the Arctic, where permafrost is thawing, glaciers are retreating and sea ice is melting. These physical changes are not only affecting large predators like polar bears, but also microscopic organisms such as Bacteria and Archaea. The impacts on microbes are far more concerning, as they are the main drivers of global biogeochemical cycles. Microbial-driven degradation of recently thawed permafrost organic matter is causing the release of critical greenhouse gases, including methane (CH4) and carbon dioxide (CO2). Parts of this formerly preserved organic carbon pool is upon thaw transported into marine systems, affecting the structure and dynamics of marine microbial communities. This thesis addresses the extensive implications of thawing permafrost on Arctic microbes. I investigated not only the microbial community composition and processes directly within the soil, but also the indirect effects of permafrost derived carbon run-off on the marine microbial structure, function and activity. By analyzing the microbial community composition, using high-throughput 16S rRNA gene sequencing, new insights on how microbial communities are structured in permafrost (Paper I), in a run-off affected fjord system (Paper II) and the Arctic Ocean (Paper IV and V) were revealed. 16S rRNA gene sequencing was also used to elucidate how permafrost derived organic matter affected the community structure and activity of coastal microbial communities (Paper III). Together, these results improve our understanding on how microbial community patterns can be used to explain biochemical processes like carbon degradation (Paper I, II, III and IV). We analyzed shifts in community composition due to climate change processes like permafrost thawing (Paper I) and carbon run-off (Paper III), thereby providing insights on which organisms and processes will be sensitive to the changes in a warmer Arctic. Permafrost is increasingly thawing, which will stimulate microbial activity, and subsequently cause the release of greenhouse gases to the atmosphere. In Paper I, we analyzed the microbial community composition every 3 cm along a 2-meter permafrost core, in order to better understand the connection between the active layer and the permafrost layer. The microbial community in the active layer was diverse and gradually shifting until a distinctive transition zone, where the phylum Bacteroidetes dominated. This short transition zone was followed by a different permafrost layer, which was dominated by a single Actinobacteria family (Intrasporangiaceae). We also performed activity measurements along the various layers, where we tested the implications of thaw. These experiments demonstrated a quick change in community composition together with an increase of genes coding for proteins involved in carbon degradation, which was leading to increased CO2 production. Terrestrial dissolved organic matter (tDOM), originating from thawing permafrost and melting glaciers, is increasingly entering the Arctic Ocean. Yet, the understanding of which fraction of tDOM is bioavailable and how fjord microbial communities respond to increases in tDOM is limited. In Paper II we investigated the DOM bioavailability in a glacial run-off affected high Arctic fjord system over time. Different DOM compounds correlated to community changes and specific indicator species, including various taxa from the order Alteromonadales were identified. The effects of permafrost derived tDOM on an Arctic fjord microbial community was tested experimentally in Paper III and we documented significant growth of one specific genus (Glaciecola) within the order Alteromonadales, due to this carbon input. This increase of Glaciecola was tightly connected with an increase of bacterial grazers, highlighting an important, yet often neglected link in the Arctic microbial food web when predicting the impact of climate change on the carbon cycle. The dynamics of microbial changes in the Arctic Ocean over a polar year was the focus of Paper IV and V. We were especially interested in the seasonal interplay between processes during the light summer and dark winter period, as this is an important driver of community composition that might be disturbed by climate change. The relative abundance of several taxa in the surface waters was found to vary with season and was associated to phytoplankton dynamics, while communities in deeper waters remained relatively unchanged. With global warming, changing surface phytoplankton growth dynamics will affect associated surface microbial communities. This will inevitably have an impact on microbial groups in the deep ocean, that are dependent on nutrients from above. One of those groups is the Thaumarchaeota, which are recognized as major contributors to marine ammonia oxidation, a crucial step in the biochemical cycling of nitrogen. The remineralization of nitrogen in the deep ocean is an important process to support the life in the surface layers. Thaumarchaeota were abundant in winter surface and deep waters throughout the year, but nearly not detectable in summer surface samples. Besides the seasonal dynamics we identified water mass to be the predominant factor in defining Thaumarchaeota community composition and not solely depth or ammonium concentration as suggested in most studies. Since their abundance is linked to water masses, a freshening of the Arctic Ocean or increased Atlantification, due to climate change, will affect Thaumarchaeota distribution. The studies included in this thesis underline the importance of microbes as the main drivers of processes that determine the balance of carbon storage and release in the Arctic and contribute to a better understanding of their role in a drastically changing environment. The results highlight the necessity of detailed microbial community analyses in order to understand how different microbes are distributed, how they interact and how they function in a globally important and changing Arctic.