A Low-Diversity Microbiota Inhabits Extreme Terrestrial Basaltic Terrains and Their Fumaroles: Implications for the Exploration of Mars

Abstract

A major objective in the exploration of Mars is to test the hypothesis that the planet hosted life. Even in the absence of life, the mapping of habitable and uninhabitable environments is an essential task in developing a complete understanding of the geological and aqueous history of Mars and, as a consequence, understanding what factors caused Earth to take a different trajectory of biological potential. We carried out the aseptic collection of samples and comparison of the bacterial and archaeal communities associated with basaltic fumaroles and rocks of varying weathering states in Hawai‘i to test four hypotheses concerning the diversity of life in these environments. Using high-throughput sequencing, we found that all these materials are inhabited by a low-diversity biota. Multivariate analyses of bacterial community data showed a clear separation between sites that have active fumaroles and other sites that comprised relict fumaroles, unaltered, and syn-emplacement basalts. Contrary to our hypothesis that high water flow environments, such as fumaroles with active mineral leaching, would be sites of high biological diversity, alpha diversity was lower in active fumaroles compared to relict or nonfumarolic sites, potentially due to high-temperature constraints on microbial diversity in fumarolic sites. A comparison of these data with communities inhabiting unaltered and weathered basaltic rocks in Idaho suggests that bacterial taxon composition of basaltic materials varies between sites, although the archaeal communities were similar in Hawai‘i and Idaho. The taxa present in both sites suggest that most of them obtain organic carbon compounds from the atmosphere and from phototrophs and that some of them, including archaeal taxa, cycle fixed nitrogen. The low diversity shows that, on Earth, extreme basaltic terrains are environments on the edge of sustaining life with implications for the biological potential of similar environments on Mars and their exploration by robots and humans.

The Case for Ancient Hot Springs in Gusev Crater, Mars

“…Where silicate materials are present, leaching removes cations and passively enriches silica, leaving a residue of opaline silica that ranges from millimeterscale coatings to complete mineral replacement of existing rocks. Fumarolic settings host microbial communities (e.g., Ellis et al, 2008;Costello et al, 2009;Benson et al, 2011;Cockell et al, 2019), but to our knowledge, their preservation over geological timescales has not been documented.…”

Mapping metabolic activity at single cell resolution in intact volcanic fumarole sediment

“…Archaeal diversity was dominated by the Thaumarchaea (94%), which accounted for 33% of all sequences. Thaumarchaea have been found in high abundance at other fumaroles (Bendia et al 2018;Cockell et al 2019) and are frequently implicated in ammonia oxidation, which enables early colonization of challenging environments and drives nitrogen cycling (Kimble et al 2018). Group 1.1c Thaumarchaea are frequently associated with acidic environments, where, due to the protonation of ammonia to ammonium, they may depend on urea hydrolysis for ammonia provisioning (Lu and Jia 2013).…”

Basaltic Terrains in Idaho and Hawai‘i as Planetary Analogs for Mars Geology and Astrobiology

“…Variations in alteration features found in cracks, gas cavities, pits, mounds, channels, and so on were highly relevant to the selection of targeted sampling locations, so each class of alteration is considered individually in the following sections. While field visual inspection and in situ analyses ( e.g ., Sehlke et al , 2019) help to identify the most attractive sample locations during field work, confirmation typically must rely on subsequent laboratory analyses of replicates ( e.g ., Cockell et al , 2019). Whether assessed during field work or in laboratory experiments, the types of alteration important to this program, in terms of temperature, process, and implied exposure times, are summarized as follows (Fig.…”