Exploring the Boundaries of Microbial Habitability in Soil

Abstract

Microbes are widely assumed to be capable of colonizing even the most challenging terrestrial surface environments on Earth given enough time. We would not expect to find surface soils uninhabited by microbes as soils typically harbor diverse microbial communities and viable microbes have been detected in soils exposed to even the most inhospitable conditions. However, if uninhabited soils do exist, we might expect to find them in Antarctica. We analyzed 204 ice‐free soils collected from across a remote valley in the Transantarctic Mountains (84–85°S, 174–177°W) and were able to identify a potential limit of microbial habitability. While most of the soils we tested contained diverse microbial communities, with fungi being particularly ubiquitous, microbes could not be detected in many of the driest, higher elevation soils—results that were confirmed using cultivation‐dependent, cultivation‐independent, and metabolic assays. While we cannot confirm that this subset of soils is completely sterile and devoid of microbial life, our results suggest that microbial life is severely restricted in the coldest, driest, and saltiest Antarctic soils. Constant exposure to these conditions for thousands of years has limited microbial communities so that their presence and activity is below detectable limits using a variety of standard methods. Such soils are unlikely to be unique to the studied region with this work supporting previous hypotheses that microbial habitability is constrained by near‐continuous exposure to cold, dry, and salty conditions, establishing the environmental conditions that limit microbial life in terrestrial surface soils.

Elevational Constraints on the Composition and Genomic Attributes of Microbial Communities in Antarctic Soils

“…Elevation is unlikely to be the sole factor driving the observed differences in microbial community structure. Instead, these results support previous hypotheses that the soil environments found at higher elevations and further inland exert increasingly strong selective pressures on soil microbial communities ( 4 , 5 , 29 ) by virtue of these higher-elevation soils being saltier, colder, and often drier. The differences in elevation may also be associated with other important variables that we were unable to measure.…”

“…Due to the ambient temperatures being well below freezing for most of the year, water availability in these soils is low, and most soils have had prolonged periods of time since the last wetting (mean age since the last wetting, ∼20,000 years) ( 2 ). In general, higher-elevation soils were farther from the Ross Ice Shelf, drier (based on the age of the last wetting as estimated by Diaz et al [ 2 ]), and saltier and contained less organic carbon ( 2 , 29 ). We note that all 10 of the soil and site variables used for downstream analyses (see Materials and Methods) were positively correlated with elevation ( r > 0.5; P < 0.05), although for NH 3 , SiO 2 , and Cl − , this correlation was weaker ( r < 0.25; P < 0.05) (see Fig.…”

“…Only 167 of the 204 soil samples yielded a sufficient number of prokaryotic 16S rRNA gene reads from the amplicon sequencing effort for inclusion in downstream analyses (see Materials and Methods) ( 29 ). The prokaryotic taxa with the highest relative abundances across these 167 soil samples included those assigned to the bacterial phyla Actinobacteria , Acidobacteria , Bacteriodetes , and Proteobacteria ( Fig.…”

“…For example, in Antarctic soils, elevation has been positively correlated with increases in UV radiation, decreases in temperature, and a decrease in available water (increased age of the last wetting estimated from concentrations of water-soluble salts) ( 2 , 5 ). These variables are difficult to measure in this remote area where visits are short and infrequent, but all of these variables have been shown to have potentially important effects on Antarctic soil communities ( 2 , 6 , 29 – 31 ).…”

“…Documenting how the genomic attributes of microbial communities vary across Antarctic soils can contribute important insights into the functional capabilities and adaptations of these unique microbial communities. Based on previous work, we predict that the microbial communities from soil samples collected further inland, i.e., those exposed to more challenging conditions, would be less diverse than those closer to the coast, with regard to both their taxonomic and their functional diversity ( 23 , 24 , 29 ). We also expected that soil communities found further inland at higher elevations would contain more specialized taxa with unique metabolic capabilities, including an increased reliance on trace gas metabolism, that allow them to persist under more resource-limited and challenging environmental conditions.…”