An Ionic Limit to Life in the Deep Subsurface.

Samuel J Payler,Mark G Fox-Powell,Sean M Paling,Jennifer F Biddle,Charles S Cockell,Barbara Sherwood Lollar,Bryne T Ngwenya,Thomas Edwards

doi:10.3389/fmicb.2019.00426

Samuel J Payler, Mark G Fox-Powell + Show 6 more

Open Access

https://doi.org/10.3389/fmicb.2019.00426

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Abstract

The physical and chemical factors that can limit or prevent microbial growth in the deep subsurface are not well defined. Brines from an evaporite sequence were sampled in the Boulby Mine, United Kingdom between 800 and 1300 m depth. Ionic, hydrogen and oxygen isotopic composition were used to identify two brine sources, an aquifer situated in strata overlying the mine, and another ambiguous source distinct from the regional groundwater. The ability of the brines to support microbial replication was tested with culturing experiments using a diversity of inocula. The examined brines were found to be permissive for growth, except one. Testing this brine’s physicochemical properties showed it to have low water activity and to be chaotropic, which we attribute to the high concentration of magnesium and chloride ions. Metagenomic sequencing of the brines that supported growth showed their microbial communities to be similar to each other and comparable to those found in other hypersaline environments. These data show that solutions high in dissolved ions can shape the microbial diversity of the continental deep subsurface biosphere. Furthermore, under certain circumstances, complex brines can establish a hard limit to microbial replication in the deep biosphere, highlighting the potential for subsurface uninhabitable aqueous environments at depths far shallower than a geothermally-defined limit to life.

Highlights

Several variables are often discussed when considering the limits to life in the deep subsurface, including temperature, pressure and limited energy and carbon sources
Samples to be analyzed for Total Inorganic Carbon/Total Organic Carbon (TIC/TOC) were collected in furnaced glass bottles, with the tops covered with furnaced aluminum foil and sealed with plastic screw-cap lids
Billingham and 215 brines isotopically fall in the range of most modern groundwater found in Britain, with some mixing with Pleistocene ground water. These isotopic values, combined with their geochemical similarity to the Sherwood Sandstone waters collected by Bottrell et al (1996), suggests they originated from the Sherwood Sandstone aquifer, dissolving halite during their passage through the evaporites

Summary

Introduction

Several variables are often discussed when considering the limits to life in the deep subsurface, including temperature, pressure and limited energy and carbon sources. Hydration shells around a chloride ion in a solution behave differently when Mg2+ is present instead of Na+ (Ohtaki and Radnai, 1993). The effect of such interactions on brine habitability are only just beginning to be understood. Extremes in a range of different physicochemical stressors brought about by dissolved ions have been demonstrated to preclude microbial propagation. These stressors include water activity (Tosca et al, 2008), chaotropicity (Hallsworth et al, 2007), and ionic strength (Fox-Powell et al, 2016).

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