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Tectonic processes control hot spring temperature and geochemistry, yet how this in turn shapes microbial community composition is poorly understood. Here, we present geochemical and 16 S rRNA gene sequencing data from 14 hot springs from contrasting styles of subduction along a convergent margin in the Peruvian Andes. We find that tectonic influence on hot spring temperature and geochemistry shapes microbial community composition. Hot springs in the flat-slab and back-arc regions of the subduction system had similar pH but differed in geochemistry and microbiology, with significant relationships between microbial community composition, geochemistry, and geologic setting. Flat-slab hot springs were chemically heterogeneous, had modest surface temperatures (up to 45 °C), and were dominated by members of the metabolically diverse phylum Proteobacteria. Whereas, back-arc hot springs were geochemically more homogenous, exhibited high concentrations of dissolved metals and gases, had higher surface temperatures (up to 81 °C), and host thermophilic archaeal and bacterial lineages.

 

Despite over a century of study, it is unknown if continental hydrothermal fields support high-temperature subsurface biospheres. Cinder Pool is among the deepest hot springs in Yellowstone and is widely studied due to unique sulfur geochemistry that is attributed to hydrolysis of molten elemental sulfur at ∼18 m depth that promotes several chemical reactions that maintain low sulfide, low oxygen, and a moderate pH of ∼4.0. Following ∼100 years of stability, Cinder Pool underwent extreme visual and chemical change (acidification) in 2018. Here, we show that depth-resolved geochemical and metagenomic-based microbial community analyses pre- (2016) and post-acidification (2020) indicate the changes are likely attributable to feedbacks between geological/geochemical processes, sulfur oxidation by subsurface Sulfolobales Archaea, and the disappearance of molten sulfur at depth. These findings underscore the dynamic and rapid feedback between the geosphere and biosphere in continental hydrothermal fields and suggest subsurface biospheres to be more prevalent in these systems than previously recognized.

 

The factors that influence biodiversity and productivity of hydrothermal ecosystems are not well understood. Here we investigate the relationship between fluid mixing, biodiversity, and chemosynthetic primary productivity in three co‐localized hot springs (RSW, RSN, and RSE) in Yellowstone National Park that have different geochemistry. All three springs are sourced by reduced hydrothermal fluid, but RSE and RSN receive input of vapour phase gas and oxidized groundwaters, with input of both being substantially higher in RSN. Metagenomic sequencing revealed that communities in RSN were more biodiverse than those of RSE and RSW in all dimensions evaluated. Microcosm activity assays indicate that rates of dissolved inorganic carbon (DIC) uptake were also higher in RSN than in RSE and RSW. Together, these results suggest that increased mixing of reduced volcanic fluid with oxidized fluids generates additional niche space capable of supporting increasingly biodiverse communities that are more productive. These results provide insight into the factors that generate and maintain chemosynthetic biodiversity in hydrothermal systems and that influence the distribution, abundance, and diversity of microbial life in communities supported by chemosynthesis. These factors may also extend to other ecosystems not supported by photosynthesis, including the vast subterranean biosphere and biospheres beneath ice sheets and glaciers.

 

Abstract Trace metals have been an important ingredient for life throughout Earth’s history. Here, we describe the genome-guided cultivation of a member of the elusive archaeal lineage Caldarchaeales (syn. Aigarchaeota ), Wolframiiraptor gerlachensis , and its growth dependence on tungsten. A metagenome-assembled genome (MAG) of W. gerlachensis encodes putative tungsten membrane transport systems, as well as pathways for anaerobic oxidation of sugars probably mediated by tungsten-dependent ferredoxin oxidoreductases that are expressed during growth. Catalyzed reporter deposition-fluorescence in-situ hybridization (CARD-FISH) and nanoscale secondary ion mass spectrometry (nanoSIMS) show that W. gerlachensis preferentially assimilates xylose. Phylogenetic analyses of 78 high-quality Wolframiiraptoraceae MAGs from terrestrial and marine hydrothermal systems suggest that tungsten-associated enzymes were present in the last common ancestor of extant Wolframiiraptoraceae . Our observations imply a crucial role for tungsten-dependent metabolism in the origin and evolution of this lineage, and hint at a relic metabolic dependence on this trace metal in early anaerobic thermophiles. 

ABSTRACT Little is known of how the confluence of subsurface and surface processes influences the assembly and habitability of hydrothermal ecosystems. To address this knowledge gap, the geochemical and microbial composition of a high-temperature, circumneutral hot spring in Yellowstone National Park was examined to identify the sources of solutes and their effect on the ecology of microbial inhabitants. Metagenomic analysis showed that populations comprising planktonic and sediment communities are archaeal dominated, are dependent on chemical energy (chemosynthetic), share little overlap in their taxonomic composition, and are differentiated by their inferred use of/tolerance to oxygen and mode of carbon metabolism. The planktonic community is dominated by putative aerobic/aerotolerant autotrophs, while the taxonomic composition of the sediment community is more evenly distributed and comprised of anaerobic heterotrophs. These observations are interpreted to reflect sourcing of the spring by anoxic, organic carbon-limited subsurface hydrothermal fluids and ingassing of atmospheric oxygen that selects for aerobic/aerotolerant organisms that have autotrophic capabilities in the water column. Autotrophy and consumption of oxygen by the planktonic community may influence the assembly of the anaerobic and heterotrophic sediment community. Support for this inference comes from higher estimated rates of genome replication in planktonic populations than sediment populations, indicating faster growth in planktonic populations. Collectively, these observations provide new insight into how mixing of subsurface waters and atmospheric oxygen create dichotomy in the ecology of hot spring communities and suggest that planktonic and sediment communities may have been less differentiated taxonomically and functionally prior to the rise of oxygen at ∼2.4 billion years ago (Gya). IMPORTANCE Understanding the source and availability of energy capable of supporting life in hydrothermal environments is central to predicting the ecology of microbial life on early Earth when volcanic activity was more widespread. Little is known of the substrates supporting microbial life in circumneutral to alkaline springs, despite their relevance to early Earth habitats. Using metagenomic and informatics approaches, water column and sediment habitats in a representative circumneutral hot spring in Yellowstone were shown to be dichotomous, with the former largely hosting aerobic/aerotolerant autotrophs and the latter primarily hosting anaerobic heterotrophs. This dichotomy is attributed to influx of atmospheric oxygen into anoxic deep hydrothermal spring waters. These results indicate that the ecology of microorganisms in circumneutral alkaline springs sourced by deep hydrothermal fluids was different prior to the rise of atmospheric oxygen ∼2.4 Gya, with planktonic and sediment communities likely to be less differentiated than contemporary circumneutral hot springs. 

Many Archaea produce membrane‐spanning lipids that enable life in extreme environments. These isoprenoid glycerol dibiphytanyl glycerol tetraethers (GDGTs) may contain up to eight cyclopentyl and one cyclohexyl ring, where higher degrees of cyclization are associated with more acidic, hotter or energy‐limited conditions. Recently, the genes encoding GDGT ring synthases,grsAB, were identified in two Sulfolobaceae; however, the distribution and abundance ofgrshomologs across environments inhabited by these and related organisms remain a mystery. To address this, we examined the distribution ofgrshomologs in relation to environmental temperature and pH, from thermal springs across Earth, where sequences derive from metagenomes, metatranscriptomes, single‐cell and cultivar genomes. The abundance ofgrshomologs shows a strong negative correlation to pH, but a weak positive correlation to temperature. Archaeal genomes and metagenome‐assembled genomes (MAGs) that carry two or moregrscopies are more abundant in low pH springs. We also findgrsin 12 archaeal classes, with the most representatives in Thermoproteia, followed by MAGs of the uncultured Korarchaeia, Bathyarchaeia and Hadarchaeia, while several Nitrososphaeria encodes >3 copies. Our findings highlight the key role ofgrs‐catalysed lipid cyclization in archaeal diversification across hot and acidic environments.

 

Hydrothermal systems form at divergent and convergent boundaries of lithospheric plates and within plates due to weakened crust and mantle plumes, playing host to diverse microbial ecosystems. Little is known of how differences in tectonic setting influence the geochemical and microbial compositions of these hydrothermal ecosystems. Here, coordinated geochemical and microbial community analyses were conducted on 87 high‐temperature (>65°C) water and sediment samples from hot springs in Yellowstone National Park, Wyoming, USA (n = 41; mantle plume setting), Iceland (n = 41, divergent boundary), and Japan (n = 5; convergent boundary). Region‐specific variation in geochemistry and sediment‐associated 16S rRNA gene amplicon sequence variant (ASV) composition was observed, with 16S rRNA gene assemblages being nearly completely distinguished by region and pH being the most explanatory parameter within regions. Several low abundance ASVs exhibited cosmopolitan distributions across regions, while most high‐abundance ASVs were only identified in specific regions. The presence of some cosmopolitan ASVs across regions argues against dispersal limitation primarily shaping the distribution of taxa among regions. Rather, the results point to local tectonic and geologic characteristics shaping the geochemistry of continental hydrothermal systems that then select for distinct microbial assemblages. These results provide new insights into the co‐evolution of hydrothermal systems and their microbial communities.

 

Metagenome assembled genomes (MAGs) and single amplified genomes (SAGs) affiliated with two distinct Methanobacterium lineages were recovered from subsurface fracture waters of the Samail Ophiolite, Sultanate of Oman. Lineage Type I was abundant in waters with circumneutral pH, whereas lineage Type II was abundant in hydrogen rich, hyperalkaline waters. Type I encoded proteins to couple hydrogen oxidation to CO2 reduction, typical of hydrogenotrophic methanogens. Surprisingly, Type II, which branched from the Type I lineage, lacked homologs of two key oxidative [NiFe]-hydrogenases. These functions were presumably replaced by formate dehydrogenases that oxidize formate to yield reductant and cytoplasmic CO2 via a pathway that was unique among characterized Methanobacteria, allowing cells to overcome CO2/oxidant limitation in high pH waters. This prediction was supported by microcosm-based radiotracer experiments that showed significant biological methane generation from formate, but not bicarbonate, in waters where the Type II lineage was detected in highest relative abundance. Phylogenetic analyses and variability in gene content suggested that recent and ongoing diversification of the Type II lineage was enabled by gene transfer, loss, and transposition. These data indicate that selection imposed by CO2/oxidant availability drove recent methanogen diversification into hyperalkaline waters that are heavily impacted by serpentinization.