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 do show that microbial habitability and activity can be restricted by near-continuous exposure to cold, dry, and salty conditions, establishing the environmental conditions that constrain habitability in terrestrial surface environments. Constant exposure to these conditions for thousands of years has generated uninhabited surface soil environments, with either no detectable microbes or conditions which are not suitable to sustain microbial activity. Such uninhabited soils are unlikely to be unique to the studied region with this work challenging expectations about where microbes might, or might not, be able to thrive on Earth and other planets.

Geochemical zones and environmental gradients for soils from the Central Transantarctic Mountains, Antarctica

“…Therefore, soils which have been exposed for long periods of time and have not experienced snow or ice melt, such as those from Schroeder Hill and Roberts Massif, are able to accumulate high concentrations of ClO4and ClO3 -. Interestingly, our ClO4concentrations are lower (maximum of ~1.9 g L -1 ) than the highest recorded tolerance (1.1M (~130 g L -1 ) NaClO4) for the extremotolerant bacteria Planococcus halocryophilus, yet a recent study shows no detectable biomass for Schroeder Hill samples (Dragone et al, 2020). (Per)chlorates are strong oxidizers and are well established as toxic, thus the concentrations of ClO4and ClO3might be additional, crucial indicators of habitat suitability.…”

“…Particular attention was given to total water-soluble salt concentrations, N:P ratios, and ClO4and ClO3concentrations, based on their influence on biodiversity, as determined in previous studies (e.g. Ball et al, 2018;Barrett et al, 2006b;Courtright et al, 2001;Dragone et al, 2020;Nkem et al, 2006). The geochemical data were compared to geographic parameters to understand how the physical environment influences the observed geochemical variability.…”

Geochemical zones and environmental gradients for soils from the central Transantarctic Mountains, Antarctica

“…. Hot deserts are typically viewed as one of the least biologically diverse environments, but cold deserts can often be even less diverse (Freckman and Virginia, 1998). Soils in Antarctica typically serve as end-members for low habitat suitability due to their high salt concentrations, low organic carbon, low soil moisture, and low mean annual temperatures (Courtright et al, 2001).…”

“…In the McMurdo Dry Valleys (MDV), organic matter and salt concentrations influence soil communities, where soils with higher amounts of organic carbon, lower water-soluble N : P ratios, and lower total water-soluble salt concentrations generally harbor the greatest biomass and biodiversity (Barrett et al, 2006;Bottos et al, 2020;Caruso et al, 2019;Magalhães et al, 2012). These Antarctic ecosystems are relatively simple and are among the few known soil systems where nematodes and microarthropods (Collembola, Acari) are at the top of the food chain (Freckman and Virginia, 1998;Hogg and Wall, 2012). Studies of soils in the MDV and Transantarctic Mountains (TAM) have been key to understanding ecosystem structure and function in extreme terrestrial environments (e.g., Caruso et al, 2019;Collins et al, 2019Collins et al, , 2020Convey and McInnes, 2005;Freckman and Virginia, 1998;Hodgson et al, 2010).…”

“…These Antarctic ecosystems are relatively simple and are among the few known soil systems where nematodes and microarthropods (Collembola, Acari) are at the top of the food chain (Freckman and Virginia, 1998;Hogg and Wall, 2012). Studies of soils in the MDV and Transantarctic Mountains (TAM) have been key to understanding ecosystem structure and function in extreme terrestrial environments (e.g., Caruso et al, 2019;Collins et al, 2019Collins et al, , 2020Convey and McInnes, 2005;Freckman and Virginia, 1998;Hodgson et al, 2010).…”