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Conspicuous Smooth and White Egg-Shaped Sulfur Structures on a Deep-Sea Hydrothermal Vent Formed by Sulfide-Oxidizing Bacteria.

ABSTRACT: Conspicuous egg-shaped, white, and smooth structures were observed at a hydrothermal vent site in the Guaymas Basin, Gulf of California. The gelatinous structures decomposed within hours after sampling. Scanning electron microscopy (SEM) and light microscopy showed that the structure consisted of filaments of less than 0.1 μm thickness, similar to those observed for "Candidatus Arcobacter sulfidicus." SEM-energy-dispersive X-ray spectroscopy (EDS) showed that the filaments were sulfur rich. According to 16S rRNA gene amplicon and fluorescence in situ hybridization (FISH) analyses, Arcobacter, a sulfide oxidizer that is known to produce filamentous elemental sulfur, was among the dominant species in the structure and was likely responsible for its formation. Arcobacter normally produces woolly snowflake like structures in opposed gradients of sulfide and oxygen. In the laboratory, we observed sulfide consumption in the anoxic zone of the structure, suggesting an anaerobic conversion. The sulfide oxidation and decomposition of the structure in the laboratory may be explained by dissolution of the sulfur filaments by reaction with sulfide under formation of polysulfides. IMPORTANCE At the deep-sea Guaymas Basin hydrothermal vent system, sulfide-rich hydrothermal fluids mix with oxygenated seawater, thereby providing a habitat for microbial sulfur oxidation. Microbial sulfur oxidation in the deep sea involves a variety of organisms and processes and can result in the excretion of elemental sulfur. Here, we report on conspicuous white and smooth gelatinous structures found on hot vents. These strange egg-shaped structures were often observed on previous occasions in the Guaymas Basin, but their composition and formation process were unknown. Our data suggest that the notable and highly ephemeral structure was likely formed by the well-known sulfide-oxidizing Arcobacter. While normally Arcobacter produces loose flocs or woolly layers, here smooth gel-like structures were found.

SUBMITTER: van Erk MR

PROVIDER: S-EPMC8557937 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Symbioses between metazoans and microbes involved in sulfur cycling are integral to the ability of animals to thrive within deep-sea hydrothermal vent environments; the development of such interactions is regarded as a key adaptation in enabling animals to successfully colonize vents. Microbes often colonize the surfaces of vent animals and, remarkably, these associations can also be observed intricately preserved by pyrite in the fossil record of vent environments, stretching back to the lower Paleozoic (Ordovician-early Silurian). In non-vent environments, sulfur isotopes are often employed to investigate the metabolic strategies of both modern and fossil organisms, as certain metabolic pathways of microbes, notably sulfate reduction, can produce large sulfur isotope fractionations. However, the sulfur isotopes of vent fossils, both ancient and recently mineralized, have seldom been explored, and it is not known if the pyrite-preserved vent organisms might also preserve potential signatures of their metabolisms. Here, we use high-resolution secondary ion mass spectrometry (SIMS) to investigate the sulfur isotopes of pyrites from recently mineralized and Ordovician-early Silurian tubeworm fossils with associated microbial fossils. Our results demonstrate that pyrites containing microbial fossils consistently have significantly more negative δ34 S values compared with nearby non-fossiliferous pyrites, and thus represent the first indication that the presence of microbial sulfur-cycling communities active at the time of pyrite formation influenced the sulfur isotope signatures of pyrite at hydrothermal vents. The observed depletions in δ34 S are generally small in magnitude and are perhaps best explained by sulfur isotope fractionation through a combination of sulfur-cycling processes carried out by vent microbes. These results highlight the potential for using sulfur isotopes to explore biological functional relationships within fossil vent communities, and to enhance understanding of how microbial and animal life has co-evolved to colonize vents throughout geological time.

Project description:Hydrogenovibrio bacteria are ubiquitous in global deep-sea hydrothermal vents. However, their adaptations enabling survival in these harsh environments are not well understood. In this study, we characterized the physiology and metabolic mechanisms of Hydrogenovibrio thermophilus strain S5, which was first isolated from an active hydrothermal vent chimney on the Southwest Indian Ridge. Physiological characterizations showed that it is a microaerobic chemolithomixotroph that can utilize sulfide, thiosulfate, elemental sulfur, tetrathionate, thiocyanate or hydrogen as energy sources and molecular oxygen as the sole electron acceptor. During thiosulfate oxidation, the strain produced extracellular sulfur globules 0.7-6.0 ?m in diameter that were mainly composed of elemental sulfur and carbon. Some organic substrates including amino acids, tryptone, yeast extract, casamino acids, casein, acetate, formate, citrate, propionate, tartrate, succinate, glucose and fructose can also serve as carbon sources, but growth is weaker than under CO2 conditions, indicating that strain S5 prefers to be chemolithoautotrophic. None of the tested organic carbons could function as energy sources. Growth tests under various conditions confirmed its adaption to a mesophilic mixing zone of hydrothermal vents in which vent fluid was mixed with cold seawater, preferring moderate temperatures (optimal 37°C), alkaline pH (optimal pH 8.0), microaerobic conditions (optimal 4% O2), and reduced sulfur compounds (e.g., sulfide, optimal 100 ?M). Comparative genomics showed that strain S5 possesses more complex sulfur metabolism systems than other members of genus Hydrogenovibrio. The genes encoding the intracellular sulfur oxidation protein (DsrEF) and assimilatory sulfate reduction were first reported in the genus Hydrogenovibrio. In summary, the versatility in energy and carbon sources, and unique physiological properties of this bacterium have facilitated its adaptation to deep-sea hydrothermal vent environments.

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Conspicuous Smooth and White Egg-Shaped Sulfur Structures on a Deep-Sea Hydrothermal Vent Formed by Sulfide-Oxidizing Bacteria.

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