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The flanking regions of Guaymas Basin, a young marginal rift basin located in the Gulf of California, are covered with thick sediment layers that are hydrothermally altered due to magmatic intrusions. To explore environmental controls on microbial community structure in this complex environment, we analyzed site- and depth-related patterns of microbial community composition (bacteria, archaea, and fungi) in hydrothermally influenced sediments with different thermal conditions, geochemical regimes, and extent of microbial mats. We compared communities in hot hydrothermal sediments (75-100°C at ~40 cm depth) covered by orange-pigmented Beggiatoaceae mats in the Cathedral Hill area, temperate sediments (25-30°C at ~40 cm depth) covered by yellow sulfur precipitates and filamentous sulfur oxidizers at the Aceto Balsamico location, hot sediments (>115°C at ~40 cm depth) with orange-pigmented mats surrounded by yellow and white mats at the Marker 14 location, and background, non-hydrothermal sediments (3.8°C at ~45 cm depth) overlain with ambient seawater. Whereas bacterial and archaeal communities are clearly structured by site-specific in-situ thermal gradients and geochemical conditions, fungal communities are generally structured by sediment depth. Unexpectedly, chytrid sequence biosignatures are ubiquitous in surficial sediments whereas deeper sediments contain diverse yeasts and filamentous fungi. In correlation analyses across different sites and sediment depths, fungal phylotypes correlate to each other to a much greater degree than Bacteria and Archaea do to each other or to fungi, further substantiating that site-specific in-situ thermal gradients and geochemical conditions that control bacteria and archaea do not extend to fungi.

ABSTRACT The microbial communities of marine seep sediments contain unexplored physiological and phylogenetic diversity. Here, we examined 30 bacterial metagenome-assembled genomes (MAGs) from cold seeps in the South China Sea, the Indian Ocean, the Scotian Basin, and the Gulf of Mexico, as well as from deep-sea hydrothermal sediments in the Guaymas Basin, Gulf of California. Phylogenetic analyses of these MAGs indicate that they form a distinct phylum-level bacterial lineage, which we propose as a new phylum, Candidatus Effluviviacota, in reference to its preferential occurrence at diverse seep areas. Based on tightly clustered high-quality MAGs, we propose two new genus-level candidatus taxa, Candidatus Effluvivivax and Candidatus Effluvibates. Genomic content analyses indicate that Candidatus Effluviviacota are chemoheterotrophs that harbor the Embden–Meyerhof–Parnas glycolysis pathway. They gain energy by fermenting organic substrates. Additionally, they display potential capabilities for the degradation of cellulose, hemicellulose, starch, xylan, and various peptides. Extracellular anaerobic respiration appears to rely on metals as electron acceptors, with electron transfer primarily mediated by multiheme cytochromes and by a flavin-based extracellular electron transfer (EET) mechanism that involves NADH-quinone oxidoreductase-demethylmenaquinone-synthesizing enzymes, uncharacterized membrane proteins, and flavin-binding proteins, also known as the NUO-DMK-EET-FMN complex. The heterogeneity within the Ca. Effluviviacota phylum suggests varying roles in energy metabolism among different genera. While NUO-DMK-EET-FMN electron transfer has been reported predominantly in Gram-positive bacteria, it is now identified in Ca. Effluviviacota as well. We detected the presence of genes associated with bacterial microcompartments in Ca. Effluviviacota, which can promote specific metabolic processes and protect the cytosol from toxic intermediates.IMPORTANCEThe newly discovered bacterial phylum Candidatus Effluviviacota is widespread across diverse seepage ecosystems, marine environments, and freshwater environments, with a notable preference for cold seeps. While maintaining an average abundance of approximately 1% in the global gene catalog of cold seep habitats, it has not hitherto been characterized. The metabolic versatility of Ca. Effluviviacota in anaerobic carbon, hydrogen, and metal cycling aligns with its prevalence in anoxic niches, with a preference for cold seep environments. Variations in metabolic potential between Ca. Effluvivivax and Ca. Effluvibates may contribute to shaping their respective habitat distributions.

We measured potential nitrate removal and denitrification rates in hydrothermally altered sediments inhabited by Beggiatoa mats and adjacent brown oil stained sediments from the Guaymas Basin, Gulf of California. Sediments with Beggiatoa maintained slightly higher rates of potential denitrification than did brown sediments at 31.2 (±12.1) versus 21.9 (±1.4) μM N d-1, respectively. In contrast, the nitrate removal rates in brown sediments were higher than those observed in mat-hosting sediments at 418 ± 145 versus 174 ± 74 μM N d-1, respectively. Additional experiments were conducted to assess the responses of denitrifying communities to environmental factors (i.e. nitrate, sulfide, and dissolved organic carbon (DOC) concentration). The denitrifying community had a high affinity for nitrate (Km = 137 ± 91 μΜ ΝΟ3-), in comparison to other environmental communities of denitrifiers, and were capable of high maximum rates of denitrification (vmax = 1164 ± 153 μM N d-1). The presence of sulfide resulted in significantly lower denitrification rates. Microorganisms with the potential to perform denitrification were assessed in these sediments using the bacterial16S rRNA gene and nitrous oxide reductase (nosZ) functional gene libraries. The bacterial 16S rRNA gene clone library was dominated by Epsilonproteobacteria (38%), some of which (e.g. Sulfurimonas sp.) have a potential for sulfide dependent denitrification. The nosZ clone library did not contain clones similar to pure culture denitrifiers; these clones were most closely associated with environmental clones.

The Guaymas Basin in the Gulf of California is characterized by active seafloor spreading, the rapid deposition of organic-rich sediments, steep geothermal gradients, and abundant methane of mixed thermogenic and microbial origin. Subsurface sediment samples from eight drilling sites with distinct geochemical and thermal profiles were selected for DNA extraction and PCR amplification to explore the diversity of methane-cycling archaea in the Guaymas Basin subsurface. We performed PCR amplifications with general (mcrIRD), and ANME-1 specific primers that target the alpha (α) subunit of methyl coenzyme M reductase (mcrA). Diverse ANME-1 lineages associated with anaerobic methane oxidation were detected in seven out of the eight drilling sites, preferentially around the methane-sulfate interface, and in several cases, showed preferences for specific sampling sites. Phylogenetically, most ANME-1 sequences from the Guaymas Basin subsurface were related to marine mud volcanoes, seep sites, and the shallow marine subsurface. The most frequently recovered methanogenic phylotypes were closely affiliated with the hyperthermophilic Methanocaldococcaceae, and found at the hydrothermally influenced Ringvent site. The coolest drilling site, in the northern axial trough of Guaymas Basin, yielded the greatest diversity in methanogen lineages. Our survey indicates the potential for extensive microbial methane cycling within subsurface sediments of Guaymas Basin.

Mud volcanoes transport deep fluidized sediment and their microbial communities and thus provide a window into the deep biosphere. However, mud volcanoes are commonly sampled at the surface and not probed at greater depths, with the consequence that their internal geochemistry and microbiology remain hidden from view. Urania Basin, a hypersaline seafloor basin in the Mediterranean, harbors a mud volcano that erupts fluidized mud into the brine. The vertical mud pipe was amenable to shipboard Niskin bottle and multicorer sampling and provided an opportunity to investigate the downward sequence of bacterial and archaeal communities of the Urania Basin brine, fluid mud layers and consolidated subsurface sediments using 16S rRNA gene sequencing. These microbial communities show characteristic, habitat-related trends as they change throughout the sample series, from extremely halophilic bacteria (KB1) and archaea (Halodesulfoarchaeum spp.) in the brine, toward moderately halophilic and thermophilic endospore-forming bacteria and uncultured archaeal lineages in the mud fluid, and finally ending in aromatics-oxidizing bacteria, uncultured spore formers, and heterotrophic subsurface archaea (Thermoplasmatales, Bathyarchaeota, and Lokiarcheota) in the deep subsurface sediment at the bottom of the mud volcano. Since these bacterial and archaeal lineages are mostly anaerobic heterotrophic fermenters, the microbial ecosystem in the brine and fluidized mud functions as a layered fermenter for the degradation of sedimentary biomass and hydrocarbons. By spreading spore-forming, thermophilic Firmicutes during eruptions, the Urania Basin mud volcano likely functions as a source of endospores that occur widely in cold seafloor sediments.

Hydrocarbons are degraded by specialized types of bacteria, archaea, and fungi. Their occurrence in marine hydrocarbon seeps and sediments prompted a study of their role and their potential interactions, using the hydrocarbon-rich hydrothermal sediments of Guaymas Basin in the Gulf of California as a model system. This sedimented vent site is characterized by localized hydrothermal circulation that introduces seawater sulfate into methane- and hydrocarbon-rich sediments, and thus selects for diverse hydrocarbon-degrading communities of which methane, alkane- and aromatics-oxidizing sulfate-reducing bacteria and archaea have been especially well-studied. Current molecular and cultivation surveys are detecting diverse fungi in Guaymas Basin hydrothermal sediments, and draw attention to possible fungal-bacterial interactions. In this Hypothesis and Theory article, we report on background, recent results and outcomes, and underlying hypotheses that guide current experiments on this topic in the Edgcomb and Teske labs in 2021, and that we will revisit during our ongoing investigations of bacterial, archaeal, and fungal communities in the deep sedimentary subsurface of Guaymas Basin.

The abyssal ocean covers more than half of the Earth’s surface, yet remains understudied and underappreciated. In this Perspectives article, we mark the occasion of the Deep Submergence Vehicle Alvin’s increased depth range (from 4500 to 6500 m) to highlight the scientific potential of the abyssal seafloor. From a geologic perspective, ultra-slow spreading mid-ocean ridges, Petit Spot volcanism, transform faults, and subduction zones put the full life cycle of oceanic crust on display in the abyss, revealing constructive and destructive forces over wide ranges in time and space. Geochemically, the abyssal pressure regime influences the solubility of constituents such as silica and carbonate, and extremely high-temperature fluid-rock reactions in the shallow subsurface lead to distinctive and potentially unique geochemical profiles. Microbial residents range from low-abundance, low-energy communities on the abyssal plains to fast growing thermophiles at hydrothermal vents. Given its spatial extent and position as an intermediate zone between coastal and deep hadal settings, the abyss represents a lynchpin in global-scale processes such as nutrient and energy flux, population structure, and biogeographic diversity. Taken together, the abyssal ocean contributes critical ecosystem services while facing acute and diffuse anthropogenic threats from deep-sea mining, pollution, and climate change.

Natural gas reservoirs in the oceanic subsurface sustain complex communities of anaerobic microbes. Here, Seitz et al. describe a previously unknown archaeal phylum, Helarchaeota, belonging to the Asgard superphylum and with the potential for oxidation of hydrothermally generated short-chain hydrocarbons.

Summary: We explore archaeal distributions in sedimentary subseafloor habitats of Guaymas Basin and the adjacent Sonora Margin, located in the Gulf of California, México. Sampling locations include (1) control sediments without hydrothermal or seep influence, (2) Sonora Margin sediments underlying oxygen minimum zone water, (3) compacted, highly reduced sediments from a pressure ridge with numerous seeps at the base of the Sonora Margin, and (4) sediments impacted by hydrothermal circulation at the off-axis Ringvent site. Generally, archaeal communities largely comprise Bathyarchaeal lineages, members of the Hadesarchaea, MBG-D, TMEG, and ANME-1 groups. Variations in archaeal community composition reflect locally specific environmental challenges. Background sediments are divided into surface and subsurface niches. Overall, the environmental setting and history of a particular site, not isolated biogeochemical properties out of context, control the subseafloor archaeal communities in Guaymas Basin and Sonora Margin sediments.

The diversity and function of microbes inhabiting hydrothermal areas is a topic of active interest in marine microbiology. Here, the authors assemble genomes from Guaymas Basin hydrothermal sediments and describe the metabolic roles of the bacterial community, which includes five new bacterial candidate phyla