Paleo-Rock-Hosted Life on Earth and the Search on Mars: A Review and Strategy for Exploration

Abstract

Here we review published studies on the abundance and diversity of terrestrial rock-hosted life, the environments it inhabits, the evolution of its metabolisms, and its fossil biomarkers to provide guidance in the search for life on Mars. Key findings are (1) much terrestrial deep subsurface metabolic activity relies on abiotic energy-yielding fluxes and in situ abiotic and biotic recycling of metabolic waste products rather than on buried organic products of photosynthesis; (2) subsurface microbial cell concentrations are highest at interfaces with pronounced chemical redox gradients or permeability variations and do not correlate with bulk host rock organic carbon; (3) metabolic pathways for chemolithoautotrophic microorganisms evolved earlier in Earth's history than those of surface-dwelling phototrophic microorganisms; (4) the emergence of the former occurred at a time when Mars was habitable, whereas the emergence of the latter occurred at a time when the martian surface was not continually habitable; (5) the terrestrial rock record has biomarkers of subsurface life at least back hundreds of millions of years and likely to 3.45 Ga with several examples of excellent preservation in rock types that are quite different from those preserving the photosphere-supported biosphere. These findings suggest that rock-hosted life would have been more likely to emerge and be preserved in a martian context. Consequently, we outline a Mars exploration strategy that targets subsurface life and scales spatially, focusing initially on identifying rocks with evidence for groundwater flow and low-temperature mineralization, then identifying redox and permeability interfaces preserved within rock outcrops, and finally focusing on finding minerals associated with redox reactions and associated traces of carbon and diagnostic chemical and isotopic biosignatures. Using this strategy on Earth yields ancient rock-hosted life, preserved in the fossil record and confirmable via a suite of morphologic, organic, mineralogical, and isotopic fingerprints at micrometer scale. We expect an emphasis on rock-hosted life and this scale-dependent strategy to be crucial in the search for life on Mars.

Keywords: Biosignatures; Mars; Microbial diversity; Search for life; Subsurface life.

FIG. 1.

Subsurface biosphere habitats from left to right: Ice and Ice-Rock Interfaces host chemolithotrophs; Marine or Lake Sediments host primarily heterotrophic communities in a high-porosity environment with diffusive flux fueled by organic photosynthate in some places and chemolithotrophic oxidation in others; Ocean Ridges have advective fluids carrying reductants and oxidants, including dissolved gases from magma and water-rock reactions, and abiotic hydrocarbons are oxidized to carbonate mounds (magmatic, non-ridge systems may provide such fluxes on other planets); Deep Basaltic Crust has H₂-fueled chemolithotrophic communities powered by water-rock reactions; Continental Sedimentary Aquifers are of lower porosity than marine sediments/crust and host mixed heterotrophic and chemolithotrophic communities; and Deep Subsurface Continental aquifers in mafic and siliceous igneous and metamorphic rocks, in some cases fractured by impacts or tectonics, host microorganisms fed by products of radiolysis and water-rock reactions.

FIG. 2.

Cartoon of different microbial metabolic processes separated into Aerobic (top), Anaerobic (bottom), Heterotrophic (left), and Autotrophic (right) bins.

FIG. 3.

(A) Cell concentrations versus depth for ice sheets, subglacial sediments, and permafrost. Open squares = Tibetan glacial ice sheets; brown-filled diamonds = Siberian permafrost; blue-filled diamonds = Siberian cryopeg; light gray-filled triangles = Antarctica ice sheets and lakes; brown-filled triangles = Antarctic subglacial sediments; brown crosses = Antarctic permafrost and subglacial sediment in New Zealand; orange crosses = Canadian High Arctic and Svalbard permafrost; light blue–filled circles = Greenland ice sheet; orange-filled circle = Greenland subglacial sediment. (B) Cell concentrations versus depth for rock and soil cores from nonpolar regions. Orange-filled circle = water-saturated sediments or sedimentary rock; orange open circle = vadose zone sediments or sedimentary rock; brown squares = Chesapeake Bay Impact sediments; pink squares = Chesapeake Bay Impact impactite; black-filled orange circle = oil-gas-coal-bearing sediment or sedimentary rock; gray-filled gray diamond = water saturated rhyolitic ash; open gray diamond = deep vadose zone rhyolitic ash; open black diamond = vadose zone basaltic rock; gray-filled black diamond = water-saturated basaltic rock, which includes recent Deccan Trap data from Dutta et al. (2018); red-filled diamond = Deccan Trap granite data from Dutta et al. (2018); purple square = metamorphic rock. Rest of data are from Magnabosco et al. (2018a). Blue open circles = Atacama desert soil from Connon et al. (2007) and Lester et al. (2007). Solid and dashed lines represent the best-fit power law for subseafloor sediments proposed by Parkes et al. (2014).

FIG. 4.

Present understanding of rock-hosted life over time. The currently recognized biosignatures of rock-hosted life from Table 1 are plotted as a function of time along with the timing of development of microbial metabolisms from molecular clock techniques, as discussed in the text. Earth's geologic timescale, Earth's oxidation, and the era of surface stability of water on Mars are also shown.

FIG. 5.

Increasing scale of metabolic footprint of subsurface life. (A) Single microbial cells attached to clay minerals of a 2.8 km deep fracture zone (Wanger et al., 2006). (B) Framboidal pyrite sack with organic mineralization from 1.5 km deep borehole. White arrow points to single bacterial cell (Maclean et al., 2008). (C) Centimeter-scale “Pseudostalactite” of quartz and goethite cemented by biogenic filaments occurring in Tertiary volcanic rocks in California (Hofmann and Farmer, 2000). (D) Ferroan carbonate septarian concretions from 88.5 Ma in the Ferron Sandstone Member of the Mancos Shale Formation in Utah that are 1–4 m in diameter (McBride et al., 2003). (E) Surface diagenetic alteration zones and traces of pre-Permian faults over Velma field, Stephens County, Oklahoma, 1 mile scale bar (Al-Shaieb et al., 1994).