Nitrogen cycling and biosignatures in a hyperarid Mars analogue environment

Abstract

The hyperarid Atacama Desert is a unique Mars-analog environment with a large near-surface soil nitrate reservoir due to the lack of rainfall leaching for millennia. We investigated nitrogen (N) cycling and organic matter dynamics in this nitrate-rich terrestrial environment by analyzing the concentrations and isotopic compositions of nitrate, organic C, and organic N, coupled with microbial pathway-enzyme inferences, across a naturally occurring rainfall gradient. Nitrate deposits in sites with an annual precipitation of <10 mm carry atmospheric δ15N, δ18O, and Δ17O signatures, while these values are overprinted by biological cycling in sites with >15 mm annual precipitation. Metagenomic analyses suggest that the Atacama Desert harbors a unique biological nitrogen cycle driven by nitrifier denitrification, nitric oxide dioxygenase-driven alternative nitrification, and organic N loss pathways. Nitrate assimilation is the only nitrate consumption pathway available in the driest sites, although some hyperarid sites also support organisms with ammonia lyase- and nitric oxide synthase-driven organic N loss. Nitrifier denitrification is enhanced in the "transition zone" desert environments, which are generally hyperarid but see occasional large rainfall events, and shifts to nitric oxide dioxygenase-driven alternative nitrifications in wetter arid sites. Since extremophilic microorganisms tend to exploit all reachable nutrients, both N and O isotope fractionations during N transformations are reduced. These results suggest that N cycling on the more recent dry Mars might be dominated by nitrate assimilation that cycles atmospheric nitrate and exchanges water O during intermittent wetting, resulting stable isotope biosignatures could shift away from martian atmospheric nitrate endmember. Early wetter Mars could nurture putative life that metabolized nitrate with traceable paleoenvironmental isotopic markers similar to microbial denitrification and nitrification stored in deep subsurface.