Microbial communities in submarine permafrost and their response to permafrost degradation and warming

The Arctic region is especially impacted by global warming as temperatures in high latitude regions have increased and are predicted to further rise at levels above the global average. This is crucial to Arctic soils and the shallow shelves of the Arctic Ocean as they are underlain by permafrost. Perennially frozen ground is a habitat for a large number and great diversity of viable microorganisms, which can remain active even under freezing conditions. Warming and thawing of permafrost makes trapped soil organic carbon more accessible to microorganisms. They can transform it to the greenhouse gases carbon dioxide, methane and nitrous oxide. On the other hand, it is assumed that thawing of the frozen ground stimulates microbial activity and carbon turnover. This can lead to a positive feedback loop of warming and greenhouse gas release. Submarine permafrost covers most areas of the Siberian Arctic Shelf and contains a large though unquantified carbon pool. However, submarine permafrost is not only affected by changes in the thermal regime but by drastic changes in the geochemical composition as it formed under terrestrial conditions and was inundated by Holocene sea level rise and coastal erosion. Seawater infiltration into permafrost sediments resulted in an increase of the pore water salinity and, thus, in thawing of permafrost in the upper sediment layers even at subzero temperatures. The permafrost below, which was not affected by seawater, remained ice-bonded, but warmed through seawater heat fluxes. The objective of this thesis was to study microbial communities in submarine permafrost with a focus on their response to seawater influence and long-term warming using a combined approach of molecular biological and physicochemical analyses. The microbial abundance, community composition and structure as well as the diversity were investigated in drill cores from two locations in the Laptev Sea, which were subjected to submarine conditions for centuries to millennia. The microbial abundance was measured through total cell counts and copy numbers of the 16S rRNA gene and of functional genes. The latter comprised genes which are indicative for methane production (mcrA) and sulfate reduction (dsrB). The microbial community was characterized by high-throughput-sequencing of the 16S rRNA gene. Physicochemical analyses included the determination of the pore water geochemical and stable isotopic composition, which were used to describe the degree of seawater influence. One major outcome of the thesis is that the submarine permafrost stratified into different so-called pore water units centuries as well as millennia after inundation: (i) sediments that were mixed with seafloor sediments, (ii) sediments that were infiltrated with seawater, and (iii) sediments that were unaffected by seawater. This stratification was reflected in the submarine permafrost microbial community composition only millennia after inundation but not on time-scales of centuries. Changes in the community composition as well as abundance were used as a measure for microbial activity and the microbial response to changing thermal and geochemical conditions. The results were discussed in the context of permafrost temperature, pore water composition, paleo-climatic proxies and sediment age. The combination of permafrost warming and increasing salinity as well as permafrost warming alone resulted in a disturbance of the microbial communities at least on time-scales of centuries. This was expressed by a loss of microbial abundance and bacterial diversity. At the same time, the bacterial community of seawater unaffected but warmed permafrost was mainly determined by environmental and climatic conditions at the time of sediment deposition. A stimulating effect of warming was observed only in seawater unaffected permafrost after millennia-scale inundation, visible through increased microbial abundance and reduced amounts of substrate. Despite submarine exposure for centuries to millennia, the community of bacteria in submarine permafrost still generally resembled the community of terrestrial permafrost. It was dominated by phyla like Actinobacteria, Chloroflexi, Firmicutes, Gemmatimonadetes and Proteobacteria, which can be active under freezing conditions. Moreover, the archaeal communities of both study sites were found to harbor high abundances of marine and terrestrial anaerobic methane oxidizing archaea (ANME). Results also suggested ANME populations to be active under in situ conditions at subzero temperatures. Modeling showed that potential anaerobic oxidation of methane (AOM) could mitigate the release of almost all stored or microbially produced methane from thawing submarine permafrost. Based on the findings presented in this thesis, permafrost warming and thawing under submarine conditions as well as permafrost warming without thaw are supposed to have marginal effects on the microbial abundance and community composition, and therefore likely also on carbon mobilization and the formation of methane. Thawing under submarine conditions even stimulates AOM and thus mitigates the release of methane.