Microbial community distribution in variously altered basalts: Insights into astrobiology sample site selection
Introduction
Terrestrial basalt environments on Earth, specifically volcanic crystalline and glassy rocks, have been shown to host heterotrophic and chemolithic bacteria using e.g. iron and sulfur as energy sources (Herrera et al., 2009; Kelly et al., 2011, Kelly et al., 2014). Both syn-emplacement (alteration via interaction with volatiles during eruption and deposition) and post-depositional alteration (e.g. ambient temperature interaction with water) have been hypothesized to increase the habitability of marine and terrestrial basalts. For instance, textural changes that occur during alteration, including increases in net porosity and permeability via the dissolution of volcanic glass, may promote microbial growth (Staudigel et al., 2008; Cockell et al., 2009; Cousins, 2015). The porous structure provides protection from environmental stressors, while weathering may also increase infiltration and water-holding capacity and nutrient availability as detrital material may collect within the fractures and pore spaces (Navarre-Sitchler et al., 2015). Variable porosity can impact these factors on relatively small spatial scales (cm), and thereby impact microbial diversity as observed in soil (Vos et al., 2013; O’Brien et al., 2016) and proposed for basalts (Kelly et al., 2011). Mineralogy has also been proposed to affect microbial diversity and distribution (see Uroz et al., 2015 for an overview); post-depositional aqueous alteration of terrestrial basalt drives chemical reactions that ultimately lead to a change in mineral composition and the release of elements and nutrients that enable the increased growth of microbial populations resulting in the formation of secondary minerals such as carbonates (e.g. calcite, aragonite), clays (e.g. smectite), and zeolites (e.g. gmelinite, harmotome) (see Richardson et al., 2012; Kanakiya et al., 2017). Despite their extreme conditions, hydrothermal systems associated with volcanic terrains such as fumaroles and geothermal springs are also known to be habitable environments that may be considered analogs for early Earth or Mars environments (Stetter, 2006; Parenteau et al., 2014).
The surface of Mars is dominated by basalt (McSween et al., 2009). Evidence for hydrothermal activity on Mars associated with basaltic volcanism has been identified by the Spirit rover, e.g. Columbia Hills (Schmidt et al., 2008; Squyres et al., 2008). Hypothesized wide-spread volcanism on Mars (during Noachian to Amazonian periods) could have led to the creation of habitable environments, particularly as basaltic rocks underwent high temperature syn-emplacement alteration during eruptions, and/or ambient temperature aqueous alteration. Evidence for interaction between water and basaltic rocks on Mars has been proposed based on the detection of mineral assemblages that include clay minerals and zeolites (Haskin et al., 2005; Ehlmann et al., 2011, Ehlmann et al., 2012) and it has been suggested that similar processes have been present throughout the geologic history of Mars (Carr and Head, 2010). The detection of mineralogical and/or geological features associated with these habitats from orbit (e.g. remote sensing or hyperspectral imaging) has the potential to play a significant role in the identification and selection of target locations to be used for astrobiological investigations. When selecting potential astrobiology targets for future space missions, identification of potentially habitable environments (e.g. evidence for water) provides some guidance. However, habitable does not necessarily indicate inhabited; even within inhabited environments potential variability in biomass abundance may lead to challenges of detection. Thus, astrobiological investigations of microbial biosignatures will ideally target smaller-scale locations within those habitable regions that have the highest probability of containing remnant microbial biomass at detectable levels. Yet, studies examining how microbial biomass and diversity relate to the geochemical and geological conditions associated with basalt alteration and weathering, are generally lacking. Little work has been done to detect and constrain biosignature distribution within terrestrial basalt environments, specifically the relationship between mineralogical/geochemical parameters that can be measured from orbit and/or investigated using a rover equipped with stand-off instruments capable of identifying selected features of interest. Here we address this knowledge gap by examining microbial biomass abundance in variably altered basalts collected from two distinct Mars analog sites intended to represent both early (Hawai’i Volcanoes National Park – late Noachian/Hesperian) and late-day Mars (Craters of the Moon National Park – Amazonian) under Mars mission analog constraints as part of the Biologic Analog Science Associated with Lava Terrains (BASALT) program (see Lim et al., 2019 for an overview). The overall objective of this study was to test the hypothesis that basalts broadly categorized as altered during simulated extra-vehicular activities (EVA), had higher abundances of microbial biomass relative to unaltered basalts. Investigating the relationship between the microbial abundance and alteration states of the basalt offers insight into potential geological and geochemical features that may be used on future planetary missions to target locations for sample collection and astrobiological studies where evidence for life may have been preserved.
Intact phospholipid-derived fatty acids (PLFA) represent biomarkers of viable microbial cells in environmental samples. Phospholipids are bacterial and eukaryotic cell membrane components that degrade rapidly (days or weeks) upon death of the organism (White et al., 1979; Harvey et al., 1986; Vestal, 1988) and thus represent intact (viable) microbial cells. PLFA represent living microbial biomass and thus, are used here as a proxy to identify locations where organic biomarkers have a greater probability of preservation and detection based on a higher initial abundance of cells. The types and proportional distribution of PLFA (profile) may also be used to characterize the microbial community members as different microbial groups produce PLFA of varying structure (e.g. chain lengths, degrees of unsaturation) (Vestal and White, 1989; Zelles, 1999; Green and Scow, 2000) and/or under differing environmental conditions (e.g. temperature, pH; Cronan and Gelmann, 1979; Russell, 1990).
Section snippets
Field sites and sample collection
Two terrestrial basalt Mars analog regions of interest were investigated: Craters of the Moon National Monument and Preserve (COTM), Idaho and Hawai’i Volcanoes National Park (HVNP), representative of both late (Amazonian) and early-day Mars (Hesperian) respectively. COTM and HVNP were selected based on existing knowledge of the geochemistry and volcanic processes within these zones that makes them robust analogs for Mars enabling the exploration of differences in geologic setting, climate, and
Microbial biomass distribution
Within COTM and HVNP, the field observable and measurable features (ASD mineral scans) were used to categorize basalt samples according to alteration (Table 1). Categorization was intentionally broad to enable sample collection within the scope of the simulated EVAs that would allow for exploratory analysis of biomass trends. In some instances, vis-NIR ASD spectrometer scans were precluded due to environmental conditions (e.g. rain) or instrument availability as part of the BASALT project
Altered basalts associated with higher microbial biomass
The distribution of PLFA within two distinct Mars analog environments suggested that alteration (both high and low temperature) may play a role in microbial biomass abundance and that observable features of alteration may be used to target future astrobiological samples.
Conclusion
Results suggest that field observable indicators of alteration may be used to select basalt outcrop targets with a higher hypothesized potential for biomarker deposition and thus ultimately detection. Basalts that exhibit syn-emplacement features as well as some evidence for post-depositional ambient weathering showed high abundances of microbial biomass in COTM. Proposed targeted features include red/orange color (oxidation), friable texture, high vesicularity/porosity and mineral profiles
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Funding support was provided by a Canadian Space Agency Flights and Fieldwork for the Advancement of Science and Technology (FAST) grant to G. Slater as well as the NASA Planetary Science and Technology Through Analog Research (PSTAR) Program (NNH14ZDA001N-PSTAR) grant (14-PSTAR14_2–0007) to D. Lim and the Idaho Space Grant Consortium to C. Renner and S. Kobs Nawotniak. The science operations research conducted during BASALT deployments was approved through the NASA Johnson Space Center
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Present address: Department of Earth and Planetary Sciences, McGill University, Montreal, Quebec, Canada