Metagenomic Analysis of Stress Genes in Microbial Mat Communities from Antarctica and the High Arctic

Abstract

Polar and alpine microbial communities experience a variety of environmental stresses, including perennial cold and freezing; however, knowledge of genomic responses to such conditions is still rudimentary. We analyzed the metagenomes of cyanobacterial mats from Arctic and Antarctic ice shelves, using high-throughput pyrosequencing to test the hypotheses that consortia from these extreme polar habitats were similar in terms of major phyla and subphyla and consequently in their potential responses to environmental stresses. Statistical comparisons of the protein-coding genes showed similarities between the mats from the two poles, with the majority of genes derived from Proteobacteria and Cyanobacteria; however, the relative proportions differed, with cyanobacterial genes more prevalent in the Antarctic mat metagenome. Other differences included a higher representation of Actinobacteria and Alphaproteobacteria in the Arctic metagenomes, which may reflect the greater access to diasporas from both adjacent ice-free lands and the open ocean. Genes coding for functional responses to environmental stress (exopolysaccharides, cold shock proteins, and membrane modifications) were found in all of the metagenomes. However, in keeping with the greater exposure of the Arctic to long-range pollutants, sequences assigned to copper homeostasis genes were statistically (30%) more abundant in the Arctic samples. In contrast, more reads matching the sigma B genes were identified in the Antarctic mat, likely reflecting the more severe osmotic stress during freeze-up of the Antarctic ponds. This study underscores the presence of diverse mechanisms of adaptation to cold and other stresses in polar mats, consistent with the proportional representation of major bacterial groups. Microbial mats dominated by cyanobacteria are commonly found in extreme environments, such as geothermal springs, hypersaline basins, ultraoligotrophic ponds, and hot and cold desert soils (10,14). Cyanobacterial mats are also a dominant feature of polar lake, pond, and river ecosystems, with some of the most luxuriant communities growing on the thick ice shelves that float on Arctic and Antarctic seas (55). The stresses encountered by organisms on polar ice shelves include sparse nutrients, freezethaw cycles, bright sunlight exposure during summer, prolonged darkness during winter, salinity fluctuations, desiccation, and persistent low temperatures (29, 56). Extreme cold is an overarching stress in the polar regions because it drastically modifies the physical-chemical environment of living cells, with effects on biochemical reaction rates, substrate transport, membrane fluidity, and conformation of macromolecules, such as DNA and proteins (45, 61). Once the freezing point is crossed, there are additional physical and chemical stresses imposed by ice crystal formation, water loss, and increasing solute concentrations.Although polar ice shelf mats are visually dominated by cyanobacteria, other microorganisms, including Bacteria, Archaea, and protists, live wit...

Light-dependent microbial metabolisms drive carbon fluxes on glacier surfaces

“…Consistently, coverage of psbD (photosystem II P680 reaction center D2 protein gene) was (mean ± s.e.) 128.0 ± 9.5 on Forni and 74.5 ± 12.5 on Baltoro, similar to that reported for Arctic and Antarctic supraglacial microbial mats (Varin et al, 2013). This suggests that oxygenic photosynthesis is among the dominant metabolisms in cryoconite holes.…”

Ecology and biogeochemistry of cyanobacteria in soils, permafrost, aquatic and cryptic polar habitats

“…Factors such as habitat stability (Varin et al 2012b), as well as the interactions and activities that occur within (Tolker-Nielsen and Molin 2000), could generate the structural and compositional differences observed between lake and stream microbial mats. The physical heterogeneity intrinsic to streams and temporal heterogeneity in flow has been suggested as the cause of species accumulation and diversification and explains the coexistence of species with diverse adaptations and requirements in stream phototrophic biofilms (Larson and Passy 2013).…”

“…Planktic organisms also play a relevant role in these ecosystems (Lizotte 2008). Filamentous cyanobacteria, namely heterocytous Nostocales and non-heterocystous Oscillatoriales are critical in structuring these microbial mats (Vincent 2000); although other microbes, such as diatoms (eukaryotes) and heterotrophic bacteria are also commonly found (Varin et al 2012b;Stanish et al 2013). In addition, cyanobacteria contribute significantly to the productivity in these ecosystems (Taton et al 2003a;Koma´rek et al 2008).…”

Microbial diversity and functional capacity in polar soils

“…Actinobacteria are prominent colonists of cold soil biotopes and have been linked to a range of functional processes such as stress response and nitrogen cycling [29,30,31 ]. Recent draft genomes of Actinobacterial isolates from cold soil environments have provided some new insights into the metabolic adaptation of these bacteria to cold environments [32,33].…”

“…Copiotrophic a-and b-Proteobacteria were more responsive to shifts in nutrient status in Arctic soils than other taxa [28], supporting their proposed role as keystone taxa. Whether similar microbial community structural changes might be expected in oligotrophic Antarctic desert soils remains uncertain.Actinobacteria are prominent colonists of cold soil biotopes and have been linked to a range of functional processes such as stress response and nitrogen cycling [29,30,31 ]. Recent draft genomes of Actinobacterial isolates from cold soil environments have provided some new insights into the metabolic adaptation of these bacteria to cold environments [32,33].…”