skip to main content


Title: 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.  more » « less
Award ID(s):
1817428
NSF-PAR ID:
10378940
Author(s) / Creator(s):
; ; ; ;
Editor(s):
Gralnick, Jeffrey A.
Date Published:
Journal Name:
Microbiology Spectrum
Volume:
9
Issue:
2
ISSN:
2165-0497
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Metal sulfide minerals, including mercury sulfides (HgS), are widespread in hydrothermal vent systems where sulfur‐oxidizing microbes are prevalent. Questions remain as to the impact of mineral composition and structure on sulfur‐oxidizing microbial populations at deep‐sea hydrothermal vents, including the possible role of microbial activity in remobilizing elemental Hg from HgS. In the present study, metal sulfides varying in metal composition, structure, and surface area were incubated for 13 days on and near a diffuse‐flow hydrothermal vent at 9°50′N on the East Pacific Rise. Upon retrieval, incubated minerals were examined by scanning electron microscopy with energy‐dispersive X‐ray spectroscopy (SEM‐EDS), X‐ray diffraction (XRD), and epifluorescence microscopy (EFM). DNA was extracted from mineral samples, and the 16S ribosomal RNA gene sequenced to characterize colonizing microbes. Sulfur‐oxidizing genera common to newly exposed surfaces (Sulfurimonas, Sulfurovum, and Arcobacter) were present on all samples. Differences in their relative abundance between and within incubation sites point to constraining effects of the immediate environment and the minerals themselves. Greater variability in colonizing community composition on off‐vent samples suggests that the bioavailability of mineral‐derived sulfide (as influenced by surface area, crystal structure, and reactivity) exerted greater control on microbial colonization in the ambient environment than in the vent environment, where dissolved sulfide is more abundant. The availability of mineral‐derived sulfide as an electron donor may thus be a key control on the activity and proliferation of deep‐sea chemosynthetic communities, and this interpretation supports the potential for microbial dissolution of HgS at hydrothermal vents.

     
    more » « less
  2. Abstract

    Microbial sulfur cycling in marine sediments often occurs in environments characterized by transient chemical gradients that affect both the availability of nutrients and the activity of microbes. High turnover rates of intermediate valence sulfur compounds and the intermittent availability of oxygen in these systems greatly impact the activity of sulfur‐oxidizing micro‐organisms in particular. In this study, the thiosulfate‐oxidizing hydrothermal vent bacteriumThiomicrospira thermophilastrain EPR85 was grown in continuous culture at a range of dissolved oxygen concentrations (0.04–1.9 mM) and high pressure (5–10 MPa) in medium buffered at pH 8. Thiosulfate oxidation under these conditions produced tetrathionate, sulfate, and elemental sulfur, in contrast to previous closed‐system experiments at ambient pressure during which thiosulfate was quantitatively oxidized to sulfate. The maximum observed specific growth rate at 5 MPa pressure under unlimited O2was 0.25 hr−1. This is comparable to theμmax(0.28 hr−1) observed at low pH (<6) at ambient pressure whenT. thermophilaproduces the same mix of sulfur species. The half‐saturation constant for O2() estimated from this study was 0.2 mM (at a cell density of 105cells/ml) and was robust at all pressures tested (0.4–10 MPa), consistent with piezotolerant behavior of this strain. The cell‐specificwas determined to be 1.5 pmol O2/cell. The concentrations of products formed were correlated with oxygen availability, with tetrathionate production in excess of sulfate production at all pressure conditions tested. This study provides evidence for transient sulfur storage during times when substrate concentration exceeds cell‐specificand subsequent consumption when oxygen dropped below that threshold. These results may be common among sulfur oxidizers in a variety of environments (e.g., deep marine sediments to photosynthetic microbial mats).

     
    more » « less
  3. null (Ed.)
    International Ocean Discovery Program Expedition 385 drilled organic-rich sediments and intruded sills in the off-axis region and axial graben of the northern spreading segment of Guaymas Basin, a young marginal seafloor spreading system in the Gulf of California. Guaymas Basin is characterized by high heat flow and magmatism in the form of sill intrusions into sediments, which extends tens of kilometers off axis, in contrast with the localized volcanism found at most mid-ocean ridge spreading centers. Sill intrusions provide transient heat sources that mobilize buried sedimentary carbon, in part as methane and other hydrocarbons, and drive hydrothermal circulation. The resulting thermal and geochemical gradients shape abundance, composition, and activity of the deep subsurface biosphere of the basin. Drill sites extend over a broad region of Guaymas Basin. Adjacent Sites U1545 and U1546, located ~52 km northwest of the northern Guaymas Basin axial graben, recovered sediment successions to ~540 meters below seafloor (mbsf) (equivalent to the core depth below seafloor, Method A [CSF-A] scale), including a thin sill (a few meters thick) drilled near the bottom of Site U1545 and a massive sill (~355–430 mbsf) at Site U1546 that chemically and physically affects the surrounding sediments. Sites U1547 and U1548, located ~27 km northwest of the axial graben, were drilled to investigate an active sill-driven hydrothermal system evident at the seafloor as an 800 m wide, circular bathymetric high called Ringvent because of its outline of a ring of active vent sites. Ringvent is underlain by a thick sill at shallow depth (Site U1547). Geothermal gradients steepen toward the Ringvent periphery (Holes U1548A–U1548C), and the zones of authigenic carbonate precipitation and of highest microbial cell abundance correspondingly shallow toward the periphery. The underlying sill was drilled several times and yielded diverse igneous rock textures, sediment/sill interfaces, and alteration minerals in veins and vesicles. The Ringvent sill became the target of an integrated, interdisciplinary sampling and research effort that included geological, geochemical, and microbiological components. The thermal, lithologic, geochemical, and microbiological contrasts between the northwestern sites (U1545 and U1546) and the Ringvent sites (U1547 and U1548) form the core scientific observations informing the direct influence of sill-sediment interaction. These observations are supplemented by results from sites that exhibit persistent influence of thermally equilibrated sill intrusions, including supporting long-lived methane cold seeps, as observed at off-axis Sites U1549 and U1552, and the persistent geochemical record of hydrocarbon formation near the sill/sediment contact, as observed at the northern axial trough Site U1550, which confirms observations from Deep Sea Drilling Project (DSDP) Leg 64. Drilling at Site U1551 ~29 km southeast of the axial graben was not successful due to unstable shallow sands, but it confirmed the dominant influence of gravity-flow sedimentation processes southeast of the axial graben. The scientific outcomes of Expedition 385 will (1) revise long-held assumptions about the role of sill emplacement in subsurface carbon mobilization versus carbon retention, (2) comprehensively examine the subsurface biosphere of Guaymas Basin and its responses and adaptations to hydrothermal conditions, (3) redefine hydrothermal controls on authigenic mineral formation in sediments, and (4) yield new insights into the long term influence of sill-sediment interaction on sediments deposited at the earliest stages of seafloor spreading, that is, when spreading centers are proximal to a continental margin. The generally high quality and high degree of completeness of the shipboard data sets present opportunities for inter- and multidisciplinary collaborations during shore-based studies. In comparison to DSDP Leg 64 to Guaymas Basin in 1979, continuous availability of sophisticated drilling strategies (e.g., the advanced piston corer [APC] and half-length APC systems) and numerous analytical innovations greatly improved sample recovery and scientific yield, particularly in the areas of organic geochemistry and microbiology. For example, microbial metagenomics did not exist 40 y ago. However, these technical refinements do not change the fact that Expedition 385 in many respects builds on the foundations of understanding laid by Leg 64 drilling in Guaymas Basin. 
    more » « less
  4. null (Ed.)
    International Ocean Discovery Program (IODP) Expedition 385 drilled organic-rich sediments with sill intrusions on the flanking regions and in the northern axial graben in Guaymas Basin, a young marginal rift basin in the Gulf of California. Guaymas Basin is characterized by a widely distributed, intense heat flow and widespread off-axis magmatism expressed by a dense network of sill intrusions across the flanking regions, which is in contrast to classical mid-ocean ridge spreading centers. The numerous off-axis sills provide multiple transient heat sources that mobilize buried sedimentary carbon, in part as methane and other hydrocarbons, and drive hydrothermal circulation. The resulting thermal and geochemical gradients shape abundance, composition, and activity of the deep subsurface biosphere of the basin. Drill sites extend over the flanking regions of Guaymas Basin, covering a distance of ~81 km from the from the northwest to the southeast. Adjacent Sites U1545 and U1546 recovered the oldest and thickest sediment successions (to ~540 meters below seafloor [mbsf]; equivalent to the core depth below seafloor, Method A [CSF-A] scale), one with a thin sill (a few meters in thickness) near the drilled bottom (Site U1545), and one with a massive, deeply buried sill (~356–430 mbsf) that chemically and physically affects the surrounding sediments (Site U1546). Sites U1547 and U1548, located in the central part of the northern Guaymas Basin segment, were drilled to investigate a 600 m wide circular mound (bathymetric high) and its periphery. The dome-like structure is outlined by a ring of active vent sites called Ringvent. It is underlain by a remarkably thick sill at shallow depth (Site U1547). Hydrothermal gradients steepen at the Ringvent periphery (Holes U1548A–U1548C), which in turn shifts the zones of authigenic carbonate precipitation and of highest microbial cell abundance toward shallower depths. The Ringvent sill was drilled several times and yielded remarkably diverse igneous rock textures, sediment–sill interfaces, and hydrothermal alteration, reflected by various secondary minerals in veins and vesicles. Thus, the Ringvent sill became the target of an integrated sampling and interdisciplinary research effort that included geological, geochemical, and microbiological specialties. The thermal, lithologic, geochemical, and microbiological contrasts between the two deep northwestern sites (U1545 and U1546) and the Ringvent sites (U1547 and U1548) form the scientific centerpiece of the expedition. These observations are supplemented by results from sites that represent attenuated cold seepage conditions in the central basin (Site U1549), complex and disturbed sediments overlying sills in the northern axial trough (Site U1550), terrigenous sedimentation events on the southeastern flanking regions (Site U1551), and hydrate occurrence in shallow sediments proximal to the Sonora margin (Site U1552). The scientific outcomes of Expedition 385 will (1) revise long-held assumptions about the role of sill emplacement in subsurface carbon mobilization versus carbon retention, (2) comprehensively examine the subsurface biosphere of Guaymas Basin and its responses and adaptations to hydrothermal conditions, (3) redefine hydrothermal controls of authigenic mineral formation in sediments, and (4) yield new insights into many geochemical and geophysical aspects of both architecture and sill–sediment interaction in a nascent spreading center. The generally high quality and high degree of completeness of the shipboard datasets present opportunities for interdisciplinary and multidisciplinary collaborations during shore-based studies. In comparison to Deep Sea Drilling Project Leg 64 to Guaymas Basin in 1979, sophisticated drilling strategies (for example, the advanced piston corer [APC] and half-length APC systems) and numerous analytical innovations have greatly improved sample recovery and scientific yield, particularly in the areas of organic geochemistry and microbiology. For example, microbial genomics did not exist 40 y ago. However, these technical refinements do not change the fact that Expedition 385 will in many respects build on the foundations laid by Leg 64 for understanding Guaymas Basin, regardless of whether adjustments are required in the near future. 
    more » « less
  5. Abstract

    Life at hydrothermal vent sites is based on chemosynthetic primary producers that supply heterotrophic microorganisms with substrates and generate biomass for higher trophic levels. Often, chemoautotrophs associate with the hydrothermal vent megafauna. To investigate attached bacterial and archaeal communities on deep-sea squat lobsters, we collected ten specimens from a hydrothermal vent in the Guaymas Basin (Gulf of California). All animals were identified asMunidopsis alviscavia morphological and molecular classification, and intraspecific divergence was determined. Amplicon sequencing of microbial DNA and cDNA revealed significant differences between microbial communities on the carapaces ofM. alviscaand those in ambient sea water. Major epibiotic bacterial taxa were chemoautotrophicGammaproteobacteria, such asThiotrichaceaeandMethylococcaceae, while archaea were almost exclusively represented by sequences affiliated withCa. Nitrosopumilus. In sea water samples, Marine Group II and III archaea and organoheterotrophicAlphaproteobacteria,FlavobacteriiaandPlanctomycetaciawere more dominant. Based on the identified taxa, we assume that main metabolic processes, carried out byM. alviscaepibiota, include ammonia, methane and sulphide oxidation. Considering thatM. alviscacould benefit from sulphide detoxification by its epibiota, and that attached microbes are supplied with a stable habitat in proximity to substrate-rich hydrothermal fluids, a mutualistic host-microbe relationship appears likely.

     
    more » « less