Interactions between temperature and energy supply drive microbial communities in hydrothermal sediment

Temperature and bioavailable energy control the distribution of life on Earth, and interact with each other due to the dependency of biological energy requirements on temperature. Here we analyze how temperature-energy interactions structure sediment microbial communities in two hydrothermally active areas of Guaymas Basin. Sites from one area experience advective input of thermogenically produced electron donors by seepage from deeper layers, whereas sites from the other area are diffusion-dominated and electron donor-depleted. In both locations, Archaea dominate at temperatures >45 °C and Bacteria at temperatures <10 °C. Yet, at the phylum level and below, there are clear differences. Hot seep sites have high proportions of typical hydrothermal vent and hot spring taxa. By contrast, high-temperature sites without seepage harbor mainly novel taxa belonging to phyla that are widespread in cold subseafloor sediment. Our results suggest that in hydrothermal sediments temperature determines domain-level dominance, whereas temperature-energy interactions structure microbial communities at the phylum-level and below.

Stratigraphy and lithogeochemistry of the Goldenville horizon and associated rocks, Baie Verte Peninsula, Newfoundland

The Goldenville horizon in the Baie Verte Peninsula is an important stratigraphic horizon that hosts primary (Cambrian to Ordovician) exhalative magnetite and pyrite and was a chemical trap for younger (Silurian to Devonian) orogenic gold mineralization. The horizon is overlain by basaltic flows and volcaniclastic rocks, is intercalated with variably coloured argillites and cherts, and underlain by mafic volcaniclastic rocks; the entire stratigraphy is cut by younger fine-grained mafic dykes and coarser gabbro. Lithogeochemical signatures of the Goldenville horizon allow it to be divided into high-Fe iron formation (HIF; &amp;gt;50% Fe2O3), low-Fe iron formation (LIF; 15-50% Fe2O3), and argillite with iron minerals (AIF; &amp;lt;15% Fe2O3). These variably Fe-rich rocks have Fe-Ti-Mn-Al systematics consistent with element derivation from varying mineral contributions from hydrothermal venting and ambient detrital sedimentation. Post-Archean Australian Shale (PAAS)-normalized rare earth element (REE) signatures for the HIF samples have negative Ce anomalies and patterns similar to modern hydrothermal sediment deposited under oxygenated ocean conditions. The PAAS-normalized REE signatures of LIF samples have positive Ce anomalies, similar to hydrothermal sediment deposited under anoxic to sub-oxic conditions. The paradoxical Ce behaviour is potentially explained by the Mn geochemistry of the LIF samples. The LIF have elevated MnO contents (2.0-7.5 weight %), suggesting that Mn from hydrothermal fluids was oxidized in an oxygenated water column during hydrothermal venting, Mn-oxides then scavenged Ce from seawater, and these Mn-oxides were subsequently deposited in the hydrothermal sediment. The Mn-rich LIF samples with positive Ce anomalies are intercalated with HIF with negative Ce anomalies, both regionally and on a metre scale within drill holes. Thus, the LIF positive Ce anomaly signature may record extended and particle-specific scavenging rather than sub-oxic/redox-stratified marine conditions. Collectively, results suggest that the Cambro-Ordovician Taconic seaway along the Laurentian margin may have been completely or near-completely oxygenated at the time of Goldenville horizon deposition.

Genome- and Community-Level Interaction Insights into Carbon Utilization and Element Cycling Functions of Hydrothermarchaeota in Hydrothermal Sediment

ABSTRACT Hydrothermal vents release reduced compounds and small organic carbon compounds into the surrounding seawater, providing essential substrates for microbial growth and bioenergy transformations. Despite the wide distribution of the marine benthic group E archaea (referred to as Hydrothermarchaeota) in the hydrothermal environment, little is known about their genomic repertoires and biogeochemical significance. Here, we studied four highly complete (>80%) metagenome-assembled genomes (MAGs) from a black smoker chimney and the surrounding sulfur-rich sediments on the South Atlantic Mid-Ocean Ridge and publicly available data sets (the Integrated Microbial Genomes system of the U.S. Department of Energy-Joint Genome Institute and NCBI SRA data sets). Genomic analysis suggested a wide carbon metabolic diversity of Hydrothermarchaeota members, including the utilization of proteins, lactate, and acetate; the anaerobic degradation of aromatics; the oxidation of C1 compounds (CO, formate, and formaldehyde); the utilization of methyl compounds; CO2 incorporation by the tetrahydromethanopterin-based Wood-Ljungdahl pathway; and participation in the type III ribulose-1,5-bisphosphate carboxylase/oxygenase-based Calvin-Benson-Bassham cycle. These microbes also potentially oxidize sulfur, arsenic, and hydrogen and engage in anaerobic respiration based on sulfate reduction and denitrification. Among the 140 MAGs reconstructed from the black smoker chimney microbial community (including Hydrothermarchaeota MAGs), community-level metabolic predictions suggested a redundancy of carbon utilization and element cycling functions and interactive syntrophic and sequential utilization of substrates. These processes might make various carbon and energy sources widely accessible to the microorganisms. Further, the analysis suggested that Hydrothermarchaeota members contained important functional components obtained from the community via lateral gene transfer, becoming a distinctive clade. This might serve as a niche-adaptive strategy for metabolizing heavy metals, C1 compounds, and reduced sulfur compounds. Collectively, the analysis provides comprehensive metabolic insights into the Hydrothermarchaeota. IMPORTANCE This study provides comprehensive metabolic insights into the Hydrothermarchaeota from comparative genomics, evolution, and community-level perspectives. Members of the Hydrothermarchaeota synergistically participate in a wide range of carbon-utilizing and element cycling processes with other microorganisms in the community. We expand the current understanding of community interactions within the hydrothermal sediment and chimney, suggesting that microbial interactions based on sequential substrate metabolism are essential to nutrient and element cycling.

Genome and community-level interaction insights on wide carbon utilizing and element cycling function of Hydrothermarchaeota from hydrothermal sediment

Hydrothermal vents release reduced compounds and small organic carbons into surrounding seawaters, providing essential substrates for microbial-derived biosynthesis and bioenergy transformations. Despite the wide distribution of Marine Benthic Group-E archaea (referred to as Hydrothermarchaeota) in hydrothermal environments, little is known on their genome blueprints and ecofunctions. Here, we studied four relatively high-completeness (> 80%) metagenome-assembled genomes (MAGs) from a black smoker chimney and surrounding sulfide sediments in the Mid-Atlantic Ridge of the South Atlantic Ocean (BSmoChi-MAR) as well as publicly available datasets. Comparative genomics suggest that Hydrothermarchaeota members have versatile carbon metabolism, including assimilating proteins, lactate and acetate, degrading aromatics anaerobically, oxidizing C1 compounds (CO, formate, and formaldehyde), utilizing methyl-compounds, and incorporating CO2 by tetrahydromethanopterin-based Wood–Ljungdahl (WL) pathway and Calvin–Benson–Bassham (CBB) cycle with type III Ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO). They could oxidize sulfur, arsenic, and hydrogen, and respire anaerobically via sulfate reduction and denitrification based on genomic evidence. The redundancy of carbon utilizing and element cycling functions, and the interactive processes of syntrophic and sequential utilization of substrates from community-level metabolic prediction, enable wide accessibility of carbon and energy sources to microorganisms. Hydrothermarchaeota members derived important functional components from the community through lateral gene transfer, and became clade-distinctive on genome content, which might serve as a niche-adaptive strategy to metabolize potential heavy metals, C1 compounds, and reduced sulfur compounds.ImportanceThis study provides comprehensive metabolic insights on Hydrothermarchaeota from comparative genomics, evolution and community-level aspects. Hydrothermarchaeota synergistically participates in a wide range of carbon utilizing and element cycling processes with other microbes in the community. We expand the current understanding of community interactions within hydrothermal sediment environments, suggesting that microbial interactions driven by functions are essential to nutrient and element cycling.

Diversity of Methane-Cycling Archaea in Hydrothermal Sediment Investigated by General and Group-Specific PCR Primers

ABSTRACTThe zonation of anaerobic methane-cyclingArchaeain hydrothermal sediment of Guaymas Basin was studied by general primer pairs (mcrI, ME1/ME2, mcrIRD) targeting the alpha subunit of methyl coenzyme M reductase gene (mcrA) and by new group-specificmcrAand 16S rRNA gene primer pairs. The mcrIRD primer pair outperformed the other generalmcrAprimer pairs in detection sensitivity and phylogenetic coverage. Methanotrophic ANME-1Archaeawere the only group detected with group-specific primers only. The detection of 14mcrAlineages surpasses the diversity previously found in this location. Most phylotypes have high sequence similarities to hydrogenotrophs, methylotrophs, and anaerobic methanotrophs previously detected at Guaymas Basin or at hydrothermal vents, cold seeps, and oil reservoirs worldwide. Additionally, fivemcrAphylotypes belonging to newly defined lineages are detected. Two of these belong to deeply branching new orders, while the others are new species or genera ofMethanopyraceaeandMethermicoccaceae. Downcore diversity decreases from all groups detected in the upper 6 cm (∼2 to 40°C, sulfate measurable to 4 cm) to only two groups below 6 cm (>40°C). Despite the presence of hyperthermophilic genera (Methanopyrus,Methanocaldococcus) in cooler surface strata, no genes were detected below 10 cm (≥60°C). WhilemcrA-based and 16S rRNA gene-based community compositions are generally congruent, the deeply branchingmcrAcannot be assigned to specific 16S rRNA gene lineages. Our study indicates that even among well-studied metabolic groups and in previously characterized model environments, major evolutionary branches are overlooked. Detecting these groups by improved molecular biological methods is a crucial first step toward understanding their roles in nature.