Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems.

Microbial communities in terrestrial geothermal systems often contain chemolithoautotrophs with well-characterized distributions and metabolic capabilities. However, the extent to which organic matter produced by these chemolithoautotrophs supports heterotrophs remains largely unknown. Here we compared the abundance and activity of peptidases and carbohydrate active enzymes (CAZymes) that are predicted to be extracellular identified in metagenomic assemblies from 63 springs in the Central American and the Andean convergent margin (Argentinian backarc of the Central Volcanic Zone), as well as the plume-influenced spreading center in Iceland. All assemblies contain two orders of magnitude more peptidases than CAZymes, suggesting that the microorganisms more often use proteins for their carbon and/or nitrogen acquisition instead of complex sugars. The CAZy families in highest abundance are GH23 and CBM50, and the most abundant peptidase families are M23 and C26, all four of which degrade peptidoglycan found in bacterial cells. This implies that the heterotrophic community relies on autochthonous dead cell biomass, rather than allochthonous plant matter, for organic material. Enzymes involved in the degradation of cyanobacterial- and algal-derived compounds are in lower abundance at every site, with volcanic sites having more enzymes degrading cyanobacterial compounds and non-volcanic sites having more enzymes degrading algal compounds. Activity assays showed that many of these enzyme classes are active in these samples. High temperature sites (> 80°C) had similar extracellular carbon-degrading enzymes regardless of their province, suggesting a less well-developed population of secondary consumers at these sites, possibly connected with the limited extent of the subsurface biosphere in these high temperature sites. We conclude that in < 80°C springs, chemolithoautotrophic production supports heterotrophs capable of degrading a wide range of organic compounds that do not vary by geological province, even though the taxonomic and respiratory repertoire of chemolithoautotrophs and heterotrophs differ greatly across these regions.

Ultrahigh-precision noble gas isotope analyses reveal pervasive subsurface fractionation in hydrothermal systems.

Mantle-derived noble gases in volcanic gases are powerful tracers of terrestrial volatile evolution, as they contain mixtures of both primordial (from Earth's accretion) and secondary (e.g., radiogenic) isotope signals that characterize the composition of deep Earth. However, volcanic gases emitted through subaerial hydrothermal systems also contain contributions from shallow reservoirs (groundwater, crust, atmosphere). Deconvolving deep and shallow source signals is critical for robust interpretations of mantle-derived signals. Here, we use a novel dynamic mass spectrometry technique to measure argon, krypton, and xenon isotopes in volcanic gas with ultrahigh precision. Data from Iceland, Germany, United States (Yellowstone, Salton Sea), Costa Rica, and Chile show that subsurface isotope fractionation within hydrothermal systems is a globally pervasive and previously unrecognized process causing substantial nonradiogenic Ar-Kr-Xe isotope variations. Quantitatively accounting for this process is vital for accurately interpreting mantle-derived volatile (e.g., noble gas and nitrogen) signals, with profound implications for our understanding of terrestrial volatile evolution.

Chemolithoautotroph distributions across the subsurface of a convergent margin.

Subducting oceanic crusts release fluids rich in biologically relevant compounds into the overriding plate, fueling subsurface chemolithoautotrophic ecosystems. To understand the impact of subsurface geochemistry on microbial communities, we collected fluid and sediments from 14 natural springs across a ~200 km transect across the Costa Rican convergent margin and performed shotgun metagenomics. The resulting 404 metagenome-assembled genomes (MAGs) cluster into geologically distinct regions based on MAG abundance patterns: outer forearc-only (25% of total relative abundance), forearc/arc-only (38% of total relative abundance), and delocalized (37% of total relative abundance) clusters. In the outer forearc, Thermodesulfovibrionia, Candidatus Bipolaricaulia, and Firmicutes have hydrogenotrophic sulfate reduction and Wood-Ljungdahl (WL) carbon fixation pathways. In the forearc/arc, Anaerolineae, Ca. Bipolaricaulia, and Thermodesulfovibrionia have sulfur oxidation, nitrogen cycling, microaerophilic respiration, and WL, while Aquificae have aerobic sulfur oxidation and reverse tricarboxylic acid carbon fixation pathway. Transformation-based canonical correspondence analysis shows that MAG distribution corresponds to concentrations of aluminum, iron, nickel, dissolved inorganic carbon, and phosphate. While delocalized MAGs appear surface-derived, the subsurface chemolithoautotrophic, metabolic, and taxonomic landscape varies by the availability of minerals/metals and volcanically derived inorganic carbon. However, the WL pathway persists across all samples, suggesting that this versatile, energy-efficient carbon fixation pathway helps shape convergent margin subsurface ecosystems.

Sampling across large-scale geological gradients to study geosphere-biosphere interactions.

Despite being one of the largest microbial ecosystems on Earth, many basic open questions remain about how life exists and thrives in the deep subsurface biosphere. Much of this ambiguity is due to the fact that it is exceedingly difficult and often prohibitively expensive to directly sample the deep subsurface, requiring elaborate drilling programs or access to deep mines. We propose a sampling approach which involves collection of a large suite of geological, geochemical, and biological data from numerous deeply-sourced seeps-including lower temperature sites-over large spatial scales. This enables research into interactions between the geosphere and the biosphere, expanding the classical local approach to regional or even planetary scales. Understanding the interplay between geology, geochemistry and biology on such scales is essential for building subsurface ecosystem models and extrapolating the ecological and biogeochemical roles of subsurface microbes beyond single site interpretations. This approach has been used successfully across the Central and South American Convergent Margins, and can be applied more broadly to other types of geological regions (i.e., rifting, intraplate volcanic, and hydrothermal settings). Working across geological spatial scales inherently encompasses broad temporal scales (e.g., millions of years of volatile cycling across a convergent margin), providing access to a framework for interpreting evolution and ecosystem functions through deep time and space. We propose that tectonic interactions are fundamental to maintaining planetary habitability through feedbacks that stabilize the ecosphere, and deep biosphere studies are fundamental to understanding geo-bio feedbacks on these processes on a global scale.

Thermoplasmatales and sulfur-oxidizing bacteria dominate the microbial community at the surface water of a CO2-rich hydrothermal spring located in Tenorio Volcano National Park, Costa Rica.

Here we report the chemical and microbial characterization of the surface water of a CO2-rich hydrothermal vent known in Costa Rica as Borbollones, located at Tenorio Volcano National Park. The Borbollones showed a temperature surrounding 60 °C, a pH of 2.4 and the gas released has a composition of ~ 97% CO2, ~ 0.07% H2S, ~ 2.3% N2 and ~ 0.12% CH4. Other chemical species such as sulfate and iron were found at high levels with respect to typical fresh water bodies. Analysis by 16S rRNA gene metabarcoding revealed that in Borbollones predominates an archaeon from the order Thermoplasmatales and one bacterium from the genus Sulfurimonas. Other sulfur- (genera Thiomonas, Acidithiobacillus, Sulfuriferula, and Sulfuricurvum) and iron-oxidizing bacteria (genera Sideroxydans, Gallionella, and Ferrovum) were identified. Our results show that CO2-influenced surface water of Borbollones contains microorganisms that are usually found in acid rock drainage environments or sulfur-rich hydrothermal vents. To our knowledge, this is the first microbiological characterization of a CO2-dominated hydrothermal spring from Central America and expands our understanding of those extreme ecosystems.

Understanding and forecasting phreatic eruptions driven by magmatic degassing.

This paper examines phreatic eruptions which are driven by inputs of magma and magmatic gas. We synthesize data from several significant phreatic systems, including two in Costa Rica (Turrialba and Poás) which are currently highly active and hazardous. We define two endmember types of phreatic eruptions, the first (type 1) in which a deeper hydrothermal system fed by magmatic gases is sealed and produces overpressure sufficient to drive explosive eruptions, and the second (type 2) where magmatic gases are supplied via open-vent degassing to a near-surface hydrothermal system, vaporizing liquid water which drives the phreatic eruptions. The surficial source of type 2 eruptions is characteristic, while the source depth of type 1 eruptions is commonly greater. Hence, type 1 eruptions tend to be more energetic than type 2 eruptions. The first type of eruption we term "phreato-vulcanian", and the second we term "phreato-surtseyan". Some systems (e.g., Ruapehu, Poás) can produce both type 1 and type 2 eruptions, and all systems can undergo sealing at various timescales. We examine a number of precursory signals which appear to be important in understanding and forecasting phreatic eruptions; these include very long period events, banded tremor, and gas ratios, in particular H2S/SO2 and CO2/SO2. We propose that if these datasets are carefully integrated during a monitoring program, it may be possible to accurately forecast phreatic eruptions.

Nitrogen recycling at the Costa Rican subduction zone: The role of incoming plate structure.

Efficient recycling of subducted sedimentary nitrogen (N) back to the atmosphere through arc volcanism has been advocated for the Central America margin while at other locations mass balance considerations and N contents of high pressure metamorphic rocks imply massive addition of subducted N to the mantle and past the zones of arc magma generation. Here, we report new results of N isotope compositions with gas chemistry and noble gas compositions of forearc and arc front springs in Costa Rica to show that the structure of the incoming plate has a profound effect on the extent of N subduction into the mantle. N isotope compositions of emitted arc gases (9-11 N°) imply less subducted pelagic sediment contribution compared to farther north. The N isotope compositions (δ15N = -4.4 to 1.6‰) of forearc springs at 9-11 N° are consistent with previously reported values in volcanic centers (δ15N = -3.0 to 1.9‰). We advocate that subduction erosion enhanced by abundant seamount subduction at 9-11 N° introduces overlying forearc crustal materials into the Costa Rican subduction zone, releasing fluids with lighter N isotope signatures. This process supports the recycling of heavier N into the deep mantle in this section of the Central America margin.

Turmoil at Turrialba Volcano (Costa Rica): Degassing and eruptive processes inferred from high-frequency gas monitoring.

Eruptive activity at Turrialba Volcano (Costa Rica) has escalated significantly since 2014, causing airport and school closures in the capital city of San José. Whether or not new magma is involved in the current unrest seems probable but remains a matter of debate as ash deposits are dominated by hydrothermal material. Here we use high-frequency gas monitoring to track the behavior of the volcano between 2014 and 2015 and to decipher magmatic versus hydrothermal contributions to the eruptions. Pulses of deeply derived CO2-rich gas (CO2/Stotal > 4.5) precede explosive activity, providing a clear precursor to eruptive periods that occurs up to 2 weeks before eruptions, which are accompanied by shallowly derived sulfur-rich magmatic gas emissions. Degassing modeling suggests that the deep magmatic reservoir is ~8-10 km deep, whereas the shallow magmatic gas source is at ~3-5 km. Two cycles of degassing and eruption are observed, each attributed to pulses of magma ascending through the deep reservoir to shallow crustal levels. The magmatic degassing signals were overprinted by a fluid contribution from the shallow hydrothermal system, modifying the gas compositions, contributing volatiles to the emissions, and reflecting complex processes of scrubbing, displacement, and volatilization. H2S/SO2 varies over 2 orders of magnitude through the monitoring period and demonstrates that the first eruptive episode involved hydrothermal gases, whereas the second did not. Massive degassing (>3000 T/d SO2 and H2S/SO2 > 1) followed, suggesting boiling off of the hydrothermal system. The gas emissions show a remarkable shift to purely magmatic composition (H2S/SO2 < 0.05) during the second eruptive period, reflecting the depletion of the hydrothermal system or the establishment of high-temperature conduits bypassing remnant hydrothermal reservoirs, and the transition from phreatic to phreatomagmatic eruptive activity.