Volcanic controls on the microbial habitability of Mars‐analogue hydrothermal environments

Abstract

Due to their potential to support chemolithotrophic life, relic hydrothermal systems on Mars are a key target for astrobiological exploration. We analysed water and sediments at six geothermal pools from the rhyolitic Kerlingarfjöll and basaltic Kverkfjöll volcanoes in Iceland, to investigate the localised controls on the habitability of these systems in terms of microbial community function. Our results show that host lithology plays a minor role in pool geochemistry and authigenic mineralogy, with the system geochemistry primarily controlled by deep volcanic processes. We find that by dictating pool water pH and redox conditions, deep volcanic processes are the primary control on microbial community structure and function, with water input from the proximal glacier acting as a secondary control by regulating pool temperatures. Kerlingarfjöll pools have reduced, circum‐neutral CO2‐rich waters with authigenic calcite‐, pyrite‐ and kaolinite‐bearing sediments. The dominant metabolisms inferred from community profiles obtained by 16S rRNA gene sequencing are methanogenesis, respiration of sulphate and sulphur (S0) oxidation. In contrast, Kverkfjöll pools have oxidised, acidic (pH < 3) waters with high concentrations of SO42‐ and high argillic alteration, resulting in Al‐phyllosilicate‐rich sediments. The prevailing metabolisms here are iron oxidation, sulphur oxidation and nitrification. Where analogous ice‐fed hydrothermal systems existed on early Mars, similar volcanic processes would likely have controlled localised metabolic potential and thus habitability. Moreover, such systems offer several habitability advantages, including a localised source of metabolic redox pairs for chemolithotrophic microorganisms and accessible trace metals. Similar pools could have provided transient environments for life on Mars; when paired with surface or near‐surface ice, these habitability niches could have persisted into the Amazonian. Additionally, they offer a confined site for biosignature formation and deposition that lends itself well to in situ robotic exploration.

Biogeochemical Responses to Mixing of Glacial Meltwater and Hot Spring Discharge in the Mount St. Helens Crater

“…Mixing of the two distinct water sources could promote biological activity by introducing chemical disequilibrium that could fuel chemotrophic microbial metabolisms. Previous studies of a volcanic subglacial lake and glacially influenced volcanic lakes have found molecular evidence for chemotrophic bacteria that utilize the redox gradient between geothermal and glacial water sources by using iron, sulfide, sulfur, or hydrogen (common geothermal components) as electron donors and oxygen, sulfate, nitrate, or carbon dioxide (common glacier components) as electron acceptors (Gaidos et al., 2009; Moreras‐Marti et al., 2021). The glacier discharge we sampled was cold (0.7°C) and contained a relative abundance of compounds that are common in oxidized waters (e.g., NO 3 − and O 2 ) but few compounds that are common in reduced waters (e.g., sFe and sMn) while the opposite was observed in the warm (51.5°C) hot spring discharge.…”

“…For example, the microbes detected in a subglacial volcanic crater lake system in Iceland were related to microbes capable of using sulfide, sulfur, or hydrogen (common geothermal components) as electron donors and oxygen, sulfate, or carbon dioxide (common glacier components) as electron acceptors (Gaidos et al, 2009). Since the mixing of geothermal waters and glacier meltwater can provide life's basic requirements, such environments are high priority targets in the search for extraterrestrial life (Garcia-Lopez & Cid, 2017;Schulze-Makuch et al, 2007) and have been studied in analog research on Earth (Gaidos et al, 2004(Gaidos et al, , 2009Moreras-Marti et al, 2021).…”

“…Previous field studies suggest that volcanic chemical species are important energy and nutrient sources for cryospheric ecosystems, including snow algae communities of stratovolcanoes of the Pacific Northwest (Hamilton & Havig, 2016;Havig & Hamilton, 2019), the englacial microbial communities of a glaciated volcano on Deception Island, Antarctica (Martinez-Alonso et al, 2019), and subglacial volcanic crater lake (Gaidos et al, 2004(Gaidos et al, , 2009 and glacially fed ponds (Moreras-Marti et al, 2021) in Iceland. However, the nature of these systems often precludes access to the discrete mixing environments that exist and/or their volcanic and cryospheric end-members.…”

Tectonic and geological setting influence hot spring microbiology

“…Surface hydrothermal features (e.g., hot springs, mudpots, geyser and fumaroles) have also been investigated to evaluate the composition and geochemical influences on their microbial communities, including in the Taupo Volcanic Zone of New Zealand (Power et al, 2018), the Tengchong Volcanic Field of China (Hou et al, 2013), YNP (Colman et al, 2019; Inskeep et al, 2013; Mitchell, 2009), and Iceland (Castenholz, 1969a; Moreras‐Marti et al, 2021), among others. Overall, a growing consensus is that pH and, to a lesser extent, temperature primarily explain the distributions of microbial taxa within geothermal systems, regardless of which hydrothermal system is being considered (Boyd et al, 2010; Colman et al, 2019; Inskeep et al, 2013; Mitchell, 2009; Moreras‐Marti et al, 2021; Power et al, 2018). Nevertheless, few studies have evaluated the associations of geochemistry with microbial community compositions across hydrothermal systems that exhibit differing tectonic, geological and hydrologic settings.…”

Comparative metagenomics at Solfatara and Pisciarelli hydrothermal systems in Italy reveal that ecological differences across substrates are not ubiquitous

“…These studies have revealed that hot springs support microbial communities that are exceptionally diverse and vary in their response to physical and geochemical parameters ( Inskeep et al, 2013 ; Sharp et al, 2014 ; Lindsay et al, 2018 ; Power et al, 2018 ; Colman et al, 2019a , b ; Podar et al, 2020 ). Some studies have found pH to be the primary physical parameter that influences the microbial community composition of hot springs in Yellowstone National Park ( Boyd et al, 2010 ; Inskeep et al, 2013 ; Colman et al, 2016 , 2019a , b ), Tengchong, China ( Hou et al, 2013 ; Xie et al, 2015 ), Iceland ( Moreras-Marti et al, 2021 ), and volcanic provinces in New Zealand ( Power et al, 2018 ). In contrast, other studies have identified temperature as the most important driver of microbial community composition in hot springs ( Miller et al, 2009 ; Cole et al, 2013 ; Sharp et al, 2014 ; Podar et al, 2020 ).…”