High-Affinity Trace Gas Oxidation by Soil Microbes Reflected in Gene Distributions Around Chilean Hot Springs in the Andean Altiplano

Abstract:

The Polloquere hot springs, located in the Salar de Surire within the Andean Altiplano, represent an environment of combined extremes. The site is characterized by high elevation (~4,200 masl), sparse vegetation, aridity, salinity, and high UV flux. Based on genomic evidence from other desert and volcanically-influenced systems, it has been hypothesized that microbes in oligotrophic soils rely on trace gas scavenging as a metabolic survival strategy. Given the emission of various gas species by Polloquere, the soil communities surrounding the hot spring could similarly feed off reduced gases from the hot spring source. To assess whether atmospheric gas-oxidizing metabolisms are active at Polloquere, we collected soil samples downwind of the hot spring across a transect, with increasing radial distance. Initial gas microcosm experiments found an increase in microbial H₂ and CO uptake in samples taken farther away from the hot spring. To verify this biological interaction, we performed shotgun metagenomics, to evaluate the microbial diversity and abundance in the soils surrounding the hot spring.

Hidden Markov Models (HMMs) were constructed for the genes encoding CH₄ monooxygenase, CO dehydrogenase, and NiFe-hydrogenase, which are regularly used as biomarkers for their respective gas metabolisms (i.e., CH₄, CO, and H₂). The HMMs were used to search the metagenomic data and identify subgroups of these genes in different organisms. Group 1h NiFe-hydrogenases and Type I CO dehydrogenases are thought to include high-affinity variants of their respective gases for atmospheric uptake. We identified these high-affinity gene subgroups across all samples of the soil transect and found that gene abundance correlated with the measured microcosm gas uptake rates. Hydrogenases displayed the strongest trend with group 1h high-affinity genes comprising 0.4% of the identified hydrogenases at 0 meters and rising to 35.5% at 30 meters distance from the hot spring. These results better characterize microbial communities in oligotrophic environments and their dependence on gas substrates.