Distinct Microbial Assemblage Structure and Archaeal Diversity in Sediments of Arctic Thermokarst Lakes Differing in Methane Sources

Abstract

Developing a microbial ecological understanding of Arctic thermokarst lake sediments in a geochemical context is an essential first step toward comprehending the contributions of these systems to greenhouse gas emissions, and understanding how they may shift as a result of long term changes in climate. In light of this, we set out to study microbial diversity and structure in sediments from four shallow thermokarst lakes in the Arctic Coastal Plain of Alaska. Sediments from one of these lakes (Sukok) emit methane (CH4) of thermogenic origin, as expected for an area with natural gas reserves. However, sediments from a lake 10 km to the North West (Siqlukaq) produce CH4 of biogenic origin. Sukok and Siqlukaq were chosen among the four lakes surveyed to test the hypothesis that active CH4-producing organisms (methanogens) would reflect the distribution of CH4 gas levels in the sediments. We first examined the structure of the little known microbial community inhabiting the thaw bulb of arctic thermokarst lakes near Barrow, AK. Molecular approaches (PCR-DGGE and iTag sequencing) targeting the SSU rRNA gene and rRNA molecule were used to profile diversity, assemblage structure, and identify potentially active members of the microbial assemblages. Overall, the potentially active (rRNA dominant) fraction included taxa that have also been detected in other permafrost environments (e.g., Bacteroidetes, Actinobacteria, Nitrospirae, Chloroflexi, and others). In addition, Siqlukaq sediments were unique compared to the other sites, in that they harbored CH4-cycling organisms (i.e., methanogenic Archaea and methanotrophic Bacteria), as well as bacteria potentially involved in N cycling (e.g., Nitrospirae) whereas Sukok sediments were dominated by taxa typically involved in photosynthesis and biogeochemical sulfur (S) transformations. This study revealed a high degree of archaeal phylogenetic diversity in addition to CH4-producing archaea, which spanned nearly the phylogenetic extent of currently recognized Archaea phyla (e.g., Euryarchaeota, Bathyarchaeota, Thaumarchaeota, Woesearchaeota, Pacearchaeota, and others). Together these results shed light on expansive bacterial and archaeal diversity in Arctic thermokarst lakes and suggest important differences in biogeochemical potential in contrasting Arctic thermokarst lake sediment ecosystems.

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“…are the most frequently detected methanotrophs in various freshwater habitats, including boreal lakes [37,38]. Members of the Methylococcaceae family were also shown to be predominant in some thermokarst lakes of Alaska [29,39] and Canada [40]. Apart from aerobic methanotrophs, we detected various methylotrophic bacteria in the bottom water of the background lakes.…”

“…The relative predominance of carbon-degrading Bacteroidetes was previously shown for a number of lakes [32,44]. Betaproteobacteria and Actinobacteria are also abundant taxa [29,44]. Betaproteobacteria and Bacteriodetes in aquatic environments are associated with organic-rich substrates and prefer labile carbon [45].…”

“…Together with low in situ NO 3 − concentration, this indicated that NO 3 − did not play an important role in this ecosystem [32]. ANME-2d together with sulfate-dependent ANME-2 a/b were also detected in another Alaskan Lake Sukok [29]. The most intriguing results were obtained for Alaskan Lake Vault, where aerobic methanotrophs of the genus Methylobacter were shown to be involved in AOM.…”

“…A quarter of all archaea in the sediments of background lakes belonged to hydrogenotrophic methanogens of the genus Methanoregula and acetoclastic Methanosarcina and Methanosaeta; both groups have been commonly detected in various thermokarst lakes [29][30][31]. In general, all four known pathways for methane production (hydrogenotrophic, aceticlastic, methylotrophic, and methyl-reducing) were previously reported for permafrost-related environments, including lakes [28][29][30][31][32][33]. The low concentration of the heavy isotope in methane carbon in both bottom water and sediments (−71 /−89 ) indicated the definitely biogenic origin of this gas [34,35].…”

“…A high abundance of the Nitrosomonadales ammonia-oxidizing bacteria and members of the order Anaerolineales were found in Alaskian lakes [32]. Methane-cycling (methanogens and methanotrophs) and N-cycling (Nitrospirae) organisms developed in a lake with methane of biogenic origin, whereas, in a lake with methane of thermogenic origin, the taxa typically involved in biogeochemical sulfur transformations and photosynthesis were dominant [29].…”