Effects of hydrogeochemistry on the microbial ecology of terrestrial hot springs

Abstract

Temperature, pH, and hydrochemistry of terrestrial hot springs play a critical role in shaping thermal microbial communities. However, the interactions of biotic and abiotic factors at this terrestrial-aquatic interface are still not well understood on a global scale, and the question of how underground events influence microbial communities remains open. To answer this, 11 new samples obtained from the El Tatio geothermal field were analyzed by 16S rRNA amplicon sequencing (V4 region), along with 191 samples from previous publications obtained from the Taupo Volcanic Zone, the Yellowstone Plateau Volcanic Field, and the Eastern Tibetan Plateau, with their temperature, pH, and major ion concentration. Microbial alpha diversity was lower in acid-sulfate waters, and no significant correlations were found with temperature. However, moderate correlations were observed between chemical parameters such as pH (mostly constrained to temperatures below 70°C), SO 4 2− and abundances of members of the phyla Armatimonadota, Deinococcota, Chloroflexota, Campilobacterota, and Thermoplasmatota. pH and SO 4 2− gradients were explained by phase separation of sulfur-rich hydrothermal fluids and oxidation of reduced sulfur in the steam phase, which were identified as key processes shaping these communities. Ordination and permutational analysis of variance showed that temperature, pH, and major element hydrochemistry explain only 24% of the microbial community structure. Therefore, most of the variance remained unexplained, suggesting that other environmental or biotic factors are also involved and highlighting the environmental complexity of the ecosystem and its great potential to test niche theory ecological associated questions. IMPORTANCE This is the first approach to investigate whether geothermal processes could have an influence on the ecology of thermal microbial communities on a global scale. In addition to temperature and pH, microbial communities are structured by sulfate concentrations, which depends on the tectono-magmatic settings (such as the depth of magmatic chambers) and the local settings (such as the availability of a confining layer separating NaCl waters from steam after phase separation) and the possibility of mixing with more diluted fluids. Comparison of microbial communities from different geothermal areas by homogeneous sequence processing showed that no significant geographic distance decay was detected on the microbial communities according to Bray-Curtis, Jaccard, unweighted, and weighted Unifrac similarity/dissimilarity indices. Instead, an ancient potential divergence in the same taxonomic groups is suggested between globally distant thermal zones.

Comparing microbial populations from diverse hydrothermal features in Yellowstone National Park: hot springs and mud volcanoes

“…Specifically, a massive 16S rRNA dataset analysis of 925 individual hot springs from the Taupo Volcanic Zone in New Zealand indicates that temperature only has a significant effect on diversity above 70°C, below which pH is the primary driver ( Power et al, 2018 ). Similarly, a recent global study of microbial diversity in hot springs from around the globe also indicated that pH, along with SO 4 2− concentration and abundances of certain phyla, is moderately correlated with microbial diversity, although most microbial variance remains unexplained ( Hamilton et al, 2019 ; Barbosa et al, 2023 ). A challenge when comparing results from multiple different studies, however, is that there are a lot of different biases in different studies, especially in analytical chemistry and nucleic acid extraction methods and amplification protocols in 16S rRNA sequencing ( Lauber et al, 2010 , 2013 ; Hinlo et al, 2017 ; Colman et al, 2021 ).…”

Acidithiobacillia class members originating at sites within the Pacific Ring of Fire and other tectonically active locations and description of the novel genus ‘Igneacidithiobacillus’

“…(B) Ternary plot of the relative concentrations of major anions describing terrestrial hydrothermal systems water chemistry. Concentrations of SO₄ 2− , HCO₃ − , and Cl − were obtained from the published literature (Hose et al, 2000;Giaveno and María, 2010;Agusto, 2011;Agusto et al, 2012;Rosales Lagarde et al, 2014;Lin et al, 2015;Gaviria Reyes et al, 2016;Muñoz Lopez, 2017;D'Auria et al, 2018;Willis et al, 2019;Zhou et al, 2020b;Sriaporn et al, 2021;Sriaporn, 2022;Barbosa et al, 2023) and this study. Arisan et al 10.3389/fmicb.2024.1360268 Frontiers in Microbiology 10 frontiersin.org…”