skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Organic Stabilization of Extracellular Elemental Sulfur in a Sulfurovum-Rich Biofilm: A New Role for Extracellular Polymeric Substances?
This work shines light on the role of extracellular polymeric substance (EPS) in the formation and preservation of elemental sulfur biominerals produced by sulfur-oxidizing bacteria. We characterized elemental sulfur particles produced within a Sulfurovum -rich biofilm in the Frasassi Cave System (Italy). The particles adopt spherical and bipyramidal morphologies, and display both stable (α-S 8 ) and metastable (β-S 8 ) crystal structures. Elemental sulfur is embedded within a dense matrix of EPS, and the particles are surrounded by organic envelopes rich in amide and carboxylic groups. Organic encapsulation and the presence of metastable crystal structures are consistent with elemental sulfur organomineralization, i.e., the formation and stabilization of elemental sulfur in the presence of organics, a mechanism that has previously been observed in laboratory studies. This research provides new evidence for the important role of microbial EPS in mineral formation in the environment. We hypothesize that the extracellular organics are used by sulfur-oxidizing bacteria for the stabilization of elemental sulfur minerals outside of the cell wall as a store of chemical energy. The stabilization of energy sources (in the form of a solid electron acceptor) in biofilms is a potential new role for microbial EPS that requires further investigation.  more » « less
Award ID(s):
1840199
PAR ID:
10349970
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
Frontiers in Microbiology
Volume:
12
ISSN:
1664-302X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Gralnick, Jeffrey A. (Ed.)
    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
  2. null (Ed.)
    Biophysical cohesive particles in aquatic systems, such as extracellular polymeric substances (EPS) and clay minerals, play an important role in determining the transport of spilled oil contamination and its eventual fate, particularly given that suspended sediment and microbial activities are often prevalent and diverse in natural environments. A series of stirring jar tests have been conducted to understand the multiple structures characteristics of the oil-mineral aggregates (OMAs) and EPS-oil-mineral aggregates (EPS-OMAs). OMAs and EPS-OMAs have been successfully generated in the laboratory within artificial seawater using: Texas crude oil (Dynamic viscosity: 7.27 × 10 –3 Pa⋅s at 20°C), two natural clay minerals (Bentonite and Kaolin clay), and Xanthan gum powder (a proxy of natural EPS). A magnetic stirrer produced a homogeneous turbulent flow with a high turbulence level similar to that under natural breaking waves. High-resolution microscopy results show that EPS, kaolinite, and bentonite lead to distinguished oil floc structures because of the different stickiness character of EPS and mineral clay particles. With relatively low stickiness, kaolinite particles tend to attach to an oil droplets surface (droplet OMAs) and become dominant in small-sized flocs in the mixture sample. In contrast, the more cohesive bentonite particles stickiness could adsorb with oil droplets and are thus dominated by larger sized flocs. Biological EPS, with the highest stickiness, demonstrated that it could bond multiple small oil droplets and form a web structure trapping oil and minerals. Generally, adding EPS leads to flake/solid OMAs formation, and individual oil droplets are rarely observed. The inclusion of ESP within the matrix, also reduced the dependence of settling velocity on floc size and mineral type. 
    more » « less
  3. null (Ed.)
    Abstract Background Lagoons are common along coastlines worldwide and are important for biogeochemical element cycling, coastal biodiversity, coastal erosion protection and blue carbon sequestration. These ecosystems are frequently disturbed by weather, tides, and human activities. Here, we investigated a shallow lagoon in New England. The brackish ecosystem releases hydrogen sulfide particularly upon physical disturbance, causing blooms of anoxygenic sulfur-oxidizing phototrophs. To study the habitat, microbial community structure, assembly and function we carried out in situ experiments investigating the bloom dynamics over time. Results Phototrophic microbial mats and permanently or seasonally stratified water columns commonly contain multiple phototrophic lineages that coexist based on their light, oxygen and nutrient preferences. We describe similar coexistence patterns and ecological niches in estuarine planktonic blooms of phototrophs. The water column showed steep gradients of oxygen, pH, sulfate, sulfide, and salinity. The upper part of the bloom was dominated by aerobic phototrophic Cyanobacteria , the middle and lower parts by anoxygenic purple sulfur bacteria ( Chromatiales ) and green sulfur bacteria ( Chlorobiales ), respectively. We show stable coexistence of phototrophic lineages from five bacterial phyla and present metagenome-assembled genomes (MAGs) of two uncultured Chlorobaculum and Prosthecochloris species. In addition to genes involved in sulfur oxidation and photopigment biosynthesis the MAGs contained complete operons encoding for terminal oxidases. The metagenomes also contained numerous contigs affiliating with Microviridae viruses, potentially affecting Chlorobi . Our data suggest a short sulfur cycle within the bloom in which elemental sulfur produced by sulfide-oxidizing phototrophs is most likely reduced back to sulfide by Desulfuromonas sp . Conclusions The release of sulfide creates a habitat selecting for anoxygenic sulfur-oxidizing phototrophs, which in turn create a niche for sulfur reducers. Strong syntrophism between these guilds apparently drives a short sulfur cycle that may explain the rapid development of the bloom. The fast growth and high biomass yield of Chlorobi -affiliated organisms implies that the studied lineages of green sulfur bacteria can thrive in hypoxic habitats. This oxygen tolerance is corroborated by oxidases found in MAGs of uncultured Chlorobi . The findings improve our understanding of the ecology and ecophysiology of anoxygenic phototrophs and their impact on the coupled biogeochemical cycles of sulfur and carbon. 
    more » « less
  4. As we expand the search for life beyond Earth, a water-dominated planet, we turn our eyes to other aquatic worlds. Microbial life found in Earth’s many extreme habitats are considered useful analogs to life forms we are likely to find in extraterrestrial bodies of water. Modern-day benthic microbial mats inhabiting the low-oxygen, high-sulfur submerged sinkholes of temperate Lake Huron (Michigan, USA) and microbialites inhabiting the shallow, high-carbonate waters of subtropical Laguna Bacalar (Yucatan Peninsula, Mexico) serve as potential working models for exploration of extraterrestrial life. In Lake Huron, delicate mats comprising motile filaments of purple-pigmented cyanobacteria capable of oxygenic and anoxygenic photosynthesis and pigment-free chemosynthetic sulfur-oxidizing bacteria lie atop soft, organic-rich sediments. In Laguna Bacalar, lithification by cyanobacteria forms massive carbonate reef structures along the shoreline. Herein, we document studies of these two distinct earthly microbial mat ecosystems and ponder how similar or modified methods of study (e.g., robotics) would be applicable to prospective mat worlds in other planets and their moons (e.g., subsurface Mars and under-ice oceans of Europa). Further studies of modern-day microbial mat and microbialite ecosystems can add to the knowledge of Earth’s biodiversity and guide the search for life in extraterrestrial hydrospheres. 
    more » « less
  5. The Chicxulub crater, Mexico, is the site of the asteroid impact that led to the end-Cretaceous mass extinction. While impact events are known to be able to cause severe disruption to surface-dwelling organisms, the effects of such catastrophic perturbations on the deep biosphere are not known. Deep ocean drilling into the peak ring of the Chicxulub impact crater (IODP expedition 364) in 2016 allowed us to study the modern deep biosphere within the (a) high-porosity melt-bearing impact breccia/suevite (617-740 mbsf) emplaced within a day or so of the Cenozoic, (b) the overlying low porosity post-impact marine Cenozoic carbonates (504-617mbsf), and the impacted and fractured granitic basement (740-1334 mbsf). The microbial biomass (~10 cells/g wet weight) was highest in the upper suevite, in underlying non-granitic subvolcanic pre-impact basanite, and at the intercalation of suevite and impact melt rock. Pre-impact sterile conditions of the uplifted granitic basement rocks and mineralogical evidence of impact-induced sterilization suggest that the basement rocks have only been amenable to microbial colonization for less than 66 Myr. Enrichments at in situ 50-60 °C show the presence of heterotrophic lifestyles in the suevite and bacterial sulfate reduction extending into the top of the granitic basement. Cultivation-independent 16S diversity profiling revealed the presence of heterotrophic (fermentative) as well as autotrophic C-fixing thermophilic bacteria in the organic-rich (up to 4 wt % total organic carbon; TOC) Cenozoic sediments. The organic-lean suevite (< 0.1% TOC) showed the unique presence of sequences related to thermophilic Synechococcus (cyanobacteria) and S-oxidizing green sulfur bacteria (chlorobi), and Chloroflexi often associated with organic-poor deep-sea sediments. Alphaproteobacteria, predominated in the upper part of the granitic basement (<1000 mbsf), while putative manganeseoxidising Bacilli (Firmicutes) predominated in the melt-rich granitic basement (>1200 mbsf). Our data suggest that the catastrophe that led to the end-Cretaceous mass extinction caused geological disruption and recolonization of microbial life in the deep subsurface biosphere at the Chicxulub impact site. 
    more » « less