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ABSTRACT The microbial recycling of organic matter in marine sediments depends upon electron acceptors that are utilized based on availability and energetic yield. Since sulfate is the most abundant oxidant once oxygen has been depleted, the sulfide produced after sulfate reduction becomes an important electron donor for autotrophic microbes. The ability of sulfide to be re‐oxidized through multiple metabolic pathways and intermediates with variable oxidation states prompts investigation into which species are preferentially utilized and what are the factors that determine the fate of reduced sulfur species. Quantifying these sulfur intermediates in porewaters is a critical first step towards achieving a more complete understanding of the oxidative sulfur cycle, yet this has been accomplished in very few studies, none of which include oligotrophic sedimentary environments in the open ocean. Here we present profiles of porewater sulfur intermediates from sediments underlying oligotrophic regions of the ocean, which encompass about 75% of the ocean's surface and are characterized by low nutrient levels and productivity. Aiming at addressing uncertainties about if and how sulfide produced by the degradation of scarce sedimentary organic matter plays a role in carbon fixation in the sediment, we determine depth profiles of redox‐sensitive metals and sulfate isotope compositions and integrate these datasets with 16S rRNA microbial community composition data and solid‐phase sulfur concentrations. We did not find significant correlations between sulfur species or trace metals and specific sulfur cycling taxa, which suggests that microorganisms in pelagic and oxic sediments may be generalists utilizing flexible metabolisms to oxidize organic matter through different electron acceptors. 

Abstract Investigations of the metabolic capabilities of anaerobic protists advances our understanding of the evolution of eukaryotic life on Earth and for uncovering analogous extraterrestrial complex microbial life. Certain species of foraminiferan protists live in environments analogous to early Earth conditions when eukaryotes evolved, including sulfidic, anoxic and hypoxic sediment porewaters. Foraminifera are known to form symbioses as well as to harbor organelles from other eukaryotes (chloroplasts), possibly bolstering the host’s independence from oxygen. The full extent of foraminiferal physiological capabilities is not fully understood. To date, evidence for foraminiferal anaerobiosis was gleaned from specimens first subjected to stresses associated with removal from in situ conditions. Here, we report comprehensive gene expression analysis of benthic foraminiferal populations preserved in situ on the euxinic (anoxic and sulfidic) bathyal seafloor, thus avoiding environmental alterations associated with sample recovery, including pressure reduction, sunlight exposure, warming, and oxygenation. Metatranscriptomics, metagenome-assembled genomes, and measurements of substrate uptake were used to study the kleptoplastidic foraminifer Nonionella stella inhabiting sulfur-oxidizing bacterial mats of the Santa Barbara Basin, off California. We show N. stella energy generation under dark euxinia is unusual because it orchestrates complex metabolic pathways for ATP production and carbon fixation through the Calvin cycle. These pathways include extended glycolysis, anaerobic fermentation, sulfide oxidation, and the presence of a membrane-bound inorganic pyrophosphatase, an enzyme that hydrolyzes inorganic pyrophosphate to actively pump protons across the mitochondrial membrane. 

Discovering new deep hydrothermal vent systems is one of the biggest challenges in ocean exploration. They are a unique window to elucidate the physical, geochemical, and biological processes that occur on the seafloor and are involved in the evolution of life on Earth. In this study, we present a molecular analysis of the microbial composition within the newly discovered hydrothermal vent field,JaichMaa ‘ja ‘ag, situated in the Southern Pescadero Basin within the Gulf of California. During the cruise expedition FK181031 in 2018, 33 sediment cores were collected from various sites within the Pescadero vent fields and processed for 16S rRNA amplicon sequence variants (ASVs) and geochemical analysis. Correlative analysis of the chemical composition of hydrothermal pore fluids and microbial abundances identified several sediment-associated phyla, including Thermotogota, that appear to be enriched in sediment horizons impacted by hydrothermal fluid flow. Comparative analysis of Thermotogota with the previously exploredAukahydrothermal vent field situated 2 km away displayed broad similarity between the two locations, although at finer scales (e.g., ASV level), there were notable differences that point to core-to-core and site-level factors revealing distinct patterns of distribution and abundance within these two sediment-hosted hydrothermal vent fields. These patterns are intricately linked to the specific physical and geochemical conditions defining each vent, illuminating the complexity of this unique deep ocean chemosynthetic ecosystem.