Physiological adaptations to serpentinization in the Samail Ophiolite, Oman

Elizabeth M Fones,Eric S Boyd,Kaitlin R Rempfert,Alexis S Templeton,Daniel B Nothaft,Saroj Poudel,Daniel R Colman,Emily A Kraus,John R Spear

doi:10.1038/s41396-019-0391-2

Abstract

Hydration of ultramafic rock during the geologic process of serpentinization can generate reduced substrates that microorganisms may use to fuel their carbon and energy metabolisms. However, serpentinizing environments also place multiple constraints on microbial life by generating highly reduced hyperalkaline waters that are limited in dissolved inorganic carbon. To better understand how microbial life persists under these conditions, we performed geochemical measurements on waters from a serpentinizing environment and subjected planktonic microbial cells to metagenomic and physiological analyses. Metabolic potential inferred from metagenomes correlated with fluid type, and genes involved in anaerobic metabolisms were enriched in hyperalkaline waters. The abundance of planktonic cells and their rates of utilization of select single-carbon compounds were lower in hyperalkaline waters than alkaline waters. However, the ratios of substrate assimilation to dissimilation were higher in hyperalkaline waters than alkaline waters, which may represent adaptation to minimize energetic and physiologic stress imposed by highly reducing, carbon-limited conditions. Consistent with this hypothesis, estimated genome sizes and average oxidation states of carbon in inferred proteomes were lower in hyperalkaline waters than in alkaline waters. These data suggest that microorganisms inhabiting serpentinized waters exhibit a unique suite of physiological adaptations that allow for their persistence under these polyextremophilic conditions.

Highlights

The earliest forms of life on Earth are commonly thought to have relied on redox reactions involving hydrogen (H2) and single-carbon (C1) compounds to fuel their carbon and energy metabolisms [1]
This finding is consistent with previous reports of low cell concentrations in hyperalkaline waters of the Cedars peridotite body [13, 14] and in high H2 chimneys of the Lost City Hydrothermal Field (LCHF) [11] but contrary to findings of higher cell concentrations in hyperalkaline waters compared with freshwaters associated with the Tablelands Ophiolite [10]
Geochemical analyses performed on hyperalkaline waters collected from the Samail Ophiolite revealed low concentrations of substrates that could potentially serve as oxidants for cells, including dissolved inorganic carbon (DIC) (Table 3)

Summary

Introduction

The earliest forms of life on Earth are commonly thought to have relied on redox reactions involving hydrogen (H2) and single-carbon (C1) compounds to fuel their carbon and energy metabolisms [1]. Despite the potential for serpentinization to have fueled the metabolisms of life on early Earth, the specific adaptations that allow for life under these conditions are not well understood

Methods

Results

Conclusion