Nearing the cold-arid limits of microbial life in permafrost of an upper dry valley, Antarctica

Abstract

Some of the coldest and driest permafrost soils on Earth are located in the high-elevation McMurdo Dry Valleys (MDVs) of Antarctica, but little is known about the permafrost microbial communities other than that microorganisms are present in these valleys. Here, we describe the microbiology and habitable conditions of highly unique dry and ice-cemented permafrost in University Valley, one of the coldest and driest regions in the MDVs (1700 m above sea level; mean temperature -23 °C; no degree days above freezing), where the ice in permafrost originates from vapour deposition rather than liquid water. We found that culturable and total microbial biomass in University Valley was extremely low, and microbial activity under ambient conditions was undetectable. Our results contrast with reports from the lower-elevation Dry Valleys and Arctic permafrost soils where active microbial populations are found, suggesting that the combination of severe cold, aridity, oligotrophy of University Valley permafrost soils severely limit microbial activity and survival.

Figure 1

Temperature and chlorine salt conditions in the McMurdo Dry Valleys. The combination of low temperature (a), low salt influx (b) and low salt concentrations (c) in the stable upland zone (SUZ) of the McMurdo Dry valleys do not permit for liquid water to exist in soils in University Valley (grey band). These conditions are met in the coastal thaw zone (CTZ) and intermediate mixed zone (IMZ). Temperature data compiled from the LTER climate database (http://www.mcmlter.org). Chlorine flux and chlorine concentration data are obtained from Witherow et al. (2006).

Figure 2

University Valley permafrost core locations. (a) University Valley placement in the Dry Valleys; (b) approximate locations of the two soil profiles used in this study (yellow) and meteorological stations (red) with depth to ice table indicated; (c) soil profiles studied are shown in solid rectangles, with sample depths analysed in dashed boxes.

Figure 3

Microbial activity assay in dry and ice-cemented permafrost samples. The ¹⁴C-labelled acetate radiorespiration assays. Open symbols represent abiotic CO₂ production in killed controls. Standard error is reported here. Not shown are assays carried out at −10 °C and −15 °C that exhibited no detectable mineralization.

Figure 4

Nutrient- and biomass-amended radiorespiration assays at −5 °C. The 30-day ¹⁴C-labelled acetate radiorespiration assays amended with 10⁶ cells P. halocryophilus OR1, 3 ml H₂0, 1 mg g⁻¹ soil of NH₄Cl or 1 mg g⁻¹ soil of Ca(H₂PO₄)₂. Assays were carried out in triplicate and error bars denote s.e.

Figure 5

Sub-zero respiration of ¹⁴C acetate measured in cryptoendoliths. Open symbols are killed controls and represent abiotic release of CO₂. Bars denote s.e. of triplicate.

Figure 6

Shared OTUs between cryptoendolith and surface soils. Bacterial (a), archaeal (b) and fungal (c) shared OTUs based on 16S rRNA gene sequences. OTUs were defined at a 97% cutoff.

Figure 7

Unfrozen water content in University Valley soils. (Top) Gravimetric (unfrozen) water content as a function of temperature in University Valley soils. The black dotted line includes the error in the sensors. Grey areas show the region for interfacial water for two values of specific surface area of soil particles. Soil water content transitions from bulk to interfacial at −15 °C (red dotted line, see Supplementary Text for details). (Bottom) Yearly envelope of soil temperatures near the head of the valley as a function of depth. The black dotted line shows the ice table at 8 cm depth. Bulk water is present in the dry soils above the ice table for up to 74 h per year.