Adaptation, spatial variability, and phylogenetic characterization of methanotrophic communities in permafrost soils of the Lena Delta, Siberia

Abstract

The Lena Delta, located in north-east Siberia in the zone of continuous permafrost, is the largest delta within the circum-arctic. The natural capacity of arctic wetlands underlain by permafrost to emit methane is currently of major concern in the context of global change, because arctic permafrost is particularly susceptible to degradation. Permafrost degradation is suggested to impose huge amounts of yet stored carbon to the atmosphere and with this to cause a positive feedback on the natural methane source strength of Siberian wetlands and tundra. An understanding of the processes that determine methane emissions in these environments is therefore essential not only for present but also for future balancing and modeling of their methane fluxes, in particular with regard to the pronounced morphological heterogeneity of polygonal tundra habitats. The ability of aerobic methane oxidizing (methanotrophic) bacteria (MOB) to function as the primary sink for methane in terrestrial habitats set the frame of the present work. Its main objective was to study the ecology of MOB in morphological units that are representative for the polygonal tundra of the Lena Delta. The particular focus was on the adaptation, spatial variability, and phylogenetic characterization of MOB in relation to the changing environmental conditions of polygonal tundra environments. The community of MOB in polygonal tundra sites of the Lena Delta was observed to be specialized to the extreme temperature regime it is exposed to. Firstly, in sites where the abundance of MOB was not limited by the availability of oxygen, MOB contributed partly more than 10 % to the total number of microbial cells. Methanotrophic cell numbers were similar to those in northern peat lands and exceeded those obtained in environments with more moderate temperatures. Secondly, potential methane oxidation rates were highest at 4Ã ° C near the permafrost table indicating that a psychrophilic/psychrotolerant methanotrophic community dominates in deep active layer zones where temperatures are constantly < 2 Ã °C. Finally, the composition of the methanotrophic community in a dry polygon rim was restricted on the genus-level and displayed a (relative) dominance of representatives closely related to known psychrophilic and psychrotolerant strains. The majority of these representatives were thereby affiliated to two micro-diverse sequence clusters specific for the permafrost habitat investigated in this study. Additionally, a comparison between the species diversity of MOB near the surface and near the permafrost table in the same polygon rim revealed no difference. The diversity of MOB in polygonal tundra environments was therefore concluded to be independent of the extreme temperature gradient within the active layer.The abundance of MOB in permafrost soils of the Lena Delta varied depending on geo-morphological unit within the polygonal tundra and depending on soil depth. Compared to a polygon rim and flood plain, the abundance of MOB was two orders of magnitude lower in a water saturated polygon centre with low redox potentials despite higher methane concentrations there. Methanotrophic abundance also decreased towards the permafrost table although in-situ methane concentrations increased with soil depth. According to this, the abundance of MOB in polygonal tundra sites was suggested to primarily depend on oxygen availability and redox potentials rather than on concentrations of methane. Based on the results of this work, polygonal tundra environments of the Lena Delta are very heterogeneous habitats for MOB. The predicted permafrost degradation and shift of dry/wet site ratios within the polygonal tundra would therefore lead to a change of methanotrophic abundance and potential activity in the Lena Delta. Also, a cold-specialized methanotrophic community as detected near the permafrost table is likely restricted in the flexibility to react to changing environmental conditions, in particular considering that also the diversity of MOB was found to be low on the genus-level.