Models of Metabolic Community Structure in Martian Habitable Environments: Constraints from a Terrestrial Analog Acid-Sulfate Fumarole Environment, Cerro Negro Volcano, Nicaragua

Abstract:

Microbial habitability in extreme environments on Earth is described by microscale geochemical conditions that constrain metabolic niches in concert with long-term habitat stability that is governed by dynamic geologic processes. Using terrestrial analogs to identify habitable martian environments requires correlating microscale geochemical constraints with reconstructions of past martian environments that are based on global-scale observations. While past martian environments can be characterized by primary parameters (e.g. pH, redox, mineralogy, thermal history), microbial habitability on Earth is a complex function of both primary and derived parameters (e.g. metabolic reaction energetics, chemical & thermal gradients, flow dynamics). In recent years we have been investigating acid-sulfate fumaroles at the Mars analog site, Cerro Negro Volcano, Nicaragua, where habitability is constrained by steep thermal gradients, spatially- and temporally-variable vent dynamics, and limited water and nutrient availability. The most common niche identified thus far is found in fumaroles that host mixed photosynthetic and chemosynthetic endolithic microbial communities. One such endolith is dominated by acidic red algae (Cyanidiales), aerobic bacterial heterotrophs (Ktedonobacteria), and archaeal thermoacidophiles (Hyperthermus, Caldisphaera, and Thermofilum). An analysis of the metabolic structure suggests that primary production by the red algae supports the growth of heterotrophic thermoacidophiles. Diversification among the chemoheterotrophs with respect to temperature and oxygen tolerance suggests community adaptation to environmental gradients or variable venting dynamics. Furthermore, individual cells within the endolith are silica-encrusted, providing the possibility for biosignature formation and preservation. Putative hydrothermal environments on early Mars with similar conditions could have supported endolithic communities with comparable metabolic strategies. Even on a generally cold and dry Mars, volcanic craters likely provided long-lived warm and wet conditions that could have supported diverse assemblages of thermoacidophilic organisms with various metabolic strategies adapted to environmental conditions of acid-sulfate fumaroles.