Microbial community distribution in variously altered basalts: Insights into astrobiology sample site selection

Highlights

• Terrestrial basalts contain detectable levels of microbial phospholipid fatty acids.

• Texture and mineralogy may play a role in biomass abundance.

• Altered basalts have higher biomass than unaltered material.

• Variation in microbial community between locations but less so within flows.

• Syn-emplacement basalts with secondary weathering potential astrobiology targets.

Abstract

Terrestrial basalts represent ecological niches with the potential for microbial habitability. However, little is known about how gradients of physical and/or chemical alteration may impact the distribution of microbial biomass. If higher abundances of microbial biomass are associated with identifiable alteration features, i.e. visible from orbit or rover, such features would become an important tool in the selection of astrobiology targets for future life-detection missions. To examine the associations between biomass abundance and basalt alteration processes, phospholipid fatty acid (PLFA) biomarker analysis was used to assess microbial biomass in basalts representative of distinct alteration categories collected from two Mars analog environments: Craters of the Moon National Monument and Preserve (COTM), Idaho and Hawai’i Volcanoes National Park (HVNP), Hawai’i. PLFA concentration was generally highest in field categorized high-temperature alteration (syn-emplacement) samples within COTM, particularly in those that may have also undergone some degree of secondary weathering. Basalts from HVNP showed more variable biomass abundances, with no clear trend between altered and unaltered basalts. HVNP fumarolic deposits (both active and relict fumarole-associated samples) generally had consistently detectable biomass although temperature appeared to play a role in abundance with the highest temperate fumarole exhibiting the lowest PLFA concentration. PLFA profiles generally had high proportions of brPLFA (including biomarkers of iron- and sulfur-reducing bacteria) and indicated that basalts were dominated by heterotrophic organisms, however no clear trend between community biomarker composition and alteration type or extent was identified. Heterogeneity of microbial biomass within terrestrial basalts suggests that identification of distinct alteration features clearly linked to high biomass (biomarkers) is challenging but that altered materials (syn-emplacement and secondary weathering) and fumarolic deposits are likely promising astrobiology targets.

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).