Geochemical Controls on Microbial Community Composition From Varied Hot Spring Environments

Abstract

Although microbial studies in hot spring environments are numerous, widespread surveys of the microbial diversity of thermal features are lacking. Many studies of hot spring environments have focused on a single organism or type of spring. In order to expand our knowledge of the extent of thermophilic life, we conducted a microbial inventory of thermal features in Yellowstone National Park that included in-depth geochemical measurements. We have analyzed microbial communities from greater than 40 thermal features from across YNP by 16S rRNA gene analysis of environmental DNA. These samples span the range of temperature and pH (48.9 -86.2°C and 2.00 -9.19) encountered in the park's thermal features. By combining phylogenetic analyses with geochemical data, we attempt to determine the level of control that the geochemistry of a spring exerts on the microbial communities. The relationship between community and geochemistry is strongest when the microbial communities are compared at the genus level. Temperature and pH are correlated with community structure, but do not alone predict the type of organisms present in a spring. Additional geochemical controls include both putative metabolically informative compounds (i.e. SO = 4 and NH + 4 ) and trace elements (i.e. F, Sr, Sb). Our geochemical approach includes computation of the state of disequilibrium for coupled redox reactions that represent possible energy-yielding reactions for microbial metabolism. Often, the highest energy yields are for hydrogen and sulfur oxidation: both pathways are known to be employed by Aquificales which dominate many of the sampled springs. Our ongoing work pairs communities with site-specific energy-yield characteristics. These results suggest niche control over community structure at the genus level. However, the much weaker relationship between geochemistry and species level groups suggests other mechanisms such as dispersal between springs or in situ evolution or mutation is affecting the individual populations that comprise the communities.

Tectonic and geological setting influence hot spring microbiology

“…Variation in hot spring pH largely correlated to variation in the taxonomic composition of communities in all three regions (Supplementary Figures 5 and 6), although this was most apparent for the Icelandic and YNP communities, owing to the wider breadth of sampling in these regions. These results support previous analyses of hot spring taxonomic and functional diversity across YNP (Colman et al, 2016;Inskeep et al, 2013;Mitchell, 2009), New Zealand (Power et al, 2018), Iceland (Moreras-Marti et al, 2021, and China (Xie et al, 2015) that together indicate pH to be the dominant factor influencing community structure, often followed secondarily by hot spring temperature. Since pH (hydrogen ion concentrations) is dictated by and involved in many of the chemical reactions that occur in springs, it can be considered an 'umbrella' parameter that captures variation in the availability and speciation of sulfur, iron, arsenic, carbon, and other elements of springs that are relevant for microbial metabolism Shock et al, 2010).…”

“…Despite the positive correlation with spring pH, diversity notably peaked at slightly acidic pH values, then decreased, consistent with patterns of functional and phylogenetic diversity of YNP hot spring metagenomes that have been suggested to result from increased mixing of hydrothermal and/or meteoric water types, resulting in slightly acidic pH values Fernandes-Martins et al, 2023). These patterns are overall consistent with trends in diversity that have been reported for numerous other globally distributed hot spring systems (Miller et al, 2009;Mitchell, 2009;Power et al, 2018;Sharp et al, 2014;Upin et al, 2023), suggesting similar, perhaps universal, controls on microbial diversity across regions. Dominant taxa were also generally similar across regions, with Crenarchaeota (including the orders Desulfurococcales, Thermoproteales, Caldarchaeales and others) and Aquificota (previously the Aquificae; including the genera Thermocrinis, Sulfurihydrogenibium, Hydrogenobaculum and Hydrogenobacter) constituting the majority of the communities (Supplementary Figures 5 and 6).…”

“…Aquificota are considered the dominant primary producers in non‐photosynthetic high‐temperature hot springs, with distinct genera distributed among springs with distinct pH realms and geochemistry. In particular, Hydrogenobaculum is abundant in low pH springs, Sulfurihydrogenibium generally dominate mid‐pH sulfidic springs, and Thermocrinis / Hydrogenobacter dominate circumneutral to alkaline springs (Hou et al, 2013; Inskeep et al, 2013; Mitchell, 2009; Power et al, 2018; Reysenbach, 2005; Reysenbach et al, 2009). Nearly all isolated Aquificota strains from hot springs are capable of fixing inorganic carbon (Reysenbach et al, 2009) that is driven by the oxidation of inorganic volatiles (e.g., H 2 , H 2 S or its derivatives S 2 O 3 − and/or S 0 ) that is generally coupled to reduction of O 2 or sometimes NO 3 − (Hedlund, Murugapiran, et al, 2015; Reysenbach, 2015; Reysenbach et al, 2009).…”

“…Surface hydrothermal features (e.g., hot springs, mudpots, geyser and fumaroles) have also been investigated to evaluate the composition and geochemical influences on their microbial communities, including in the Taupo Volcanic Zone of New Zealand (Power et al, 2018), the Tengchong Volcanic Field of China (Hou et al, 2013), YNP (Colman et al, 2019; Inskeep et al, 2013; Mitchell, 2009), and Iceland (Castenholz, 1969a; Moreras‐Marti et al, 2021), among others. Overall, a growing consensus is that pH and, to a lesser extent, temperature primarily explain the distributions of microbial taxa within geothermal systems, regardless of which hydrothermal system is being considered (Boyd et al, 2010; Colman et al, 2019; Inskeep et al, 2013; Mitchell, 2009; Moreras‐Marti et al, 2021; Power et al, 2018). Nevertheless, few studies have evaluated the associations of geochemistry with microbial community compositions across hydrothermal systems that exhibit differing tectonic, geological and hydrologic settings.…”