Prevalence of trace gas-oxidizing soil bacteria increases with radial distance from Polloquere hot spring within a high-elevation Andean cold desert

Zachary K Garvin; Sebastian R Abades; Nicole Trefault; Fernando D Alfaro; Katie Sipes; Karen G Lloyd; Tullis C Onstott

doi:10.1093/ismejo/wrae062

Prevalence of trace gas-oxidizing soil bacteria increases with radial distance from Polloquere hot spring within a high-elevation Andean cold desert

ISME J. 2024 Apr 16:wrae062. doi: 10.1093/ismejo/wrae062. Online ahead of print.

Authors

Zachary K Garvin¹, Sebastian R Abades², Nicole Trefault², Fernando D Alfaro², Katie Sipes^{3

4}, Karen G Lloyd³, Tullis C Onstott¹

Affiliations

¹ Department of Geosciences, Princeton University, Princeton, NJ, United States.
² GEMA Center for Genomics, Ecology & Environment, Universidad Mayor, Camino La Pirámide, Santiago, Chile.
³ Department of Microbiology, University of Tennessee, Knoxville, Knoxville, TN, United States.
⁴ Department of Environmental Sciences, Aarhus University, Roskilde, Denmark.

PMID: 38625060
DOI: 10.1093/ismejo/wrae062

Abstract

High-elevation arid regions harbor microbial communities reliant on metabolic niches and flexibility to survive under biologically stressful conditions, including nutrient limitation that necessitates the utilization of atmospheric trace gases as electron donors. Geothermal springs present "oases" of microbial activity, diversity, and abundance by delivering water and substrates, including reduced gases. However, it is unknown whether these springs exhibit a gradient of effects, increasing the spatial reach of their impact on trace gas-oxidizing microbes in the surrounding soils. This study assessed whether proximity to Polloquere, a high-altitude geothermal spring in an Andean salt flat, alters the diversity and metabolic structure of nearby soil bacterial populations compared to the surrounding cold desert. Recovered DNA quantities and metagenomic analyses indicate that the spring represents an oasis for microbes in this challenging environment, supporting greater biomass with more diverse metabolic functions in proximal soils that declines sharply with radial distance from the spring. Despite the sharp decrease in biomass, potential rates of atmospheric hydrogen (H2) and carbon monoxide (CO) uptake increase away from the spring. Kinetic estimates suggest that this activity is due to high-affinity trace gas consumption, likely as a survival strategy for energy and/or carbon acquisition. These results demonstrate that Polloquere regulates a gradient of diverse microbial communities and metabolisms, culminating in increased activity of trace gas-oxidizers as the influence of the spring yields to that of the regional salt flat environment. This suggests that the spring holds local importance within the context of the broader salt flat and potentially represents a model ecosystem for other geothermal systems in high-altitude desert environments.

Keywords: geomicrobiology; metagenomics; microbial ecology; trace gas.