Ruff
S. Emil
Ruff
S. Emil
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ArticleMicrobial communities under distinct thermal and geochemical regimes in axial and off-axis sediments of Guaymas Basin(Frontiers Media, 2021-02-12) Teske, Andreas P. ; Wegener, Gunter ; Chanton, Jeffrey P. ; White, Dylan ; MacGregor, Barbara J. ; Hoer, Daniel ; de Beer, Dirk ; Zhuang, Guangchao ; Saxton, Matthew A. ; Joye, Samantha B. ; Lizarralde, Daniel ; Soule, S. Adam ; Ruff, S. EmilCold seeps and hydrothermal vents are seafloor habitats fueled by subsurface energy sources. Both habitat types coexist in Guaymas Basin in the Gulf of California, providing an opportunity to compare microbial communities with distinct physiologies adapted to different thermal regimes. Hydrothermally active sites in the southern Guaymas Basin axial valley, and cold seep sites at Octopus Mound, a carbonate mound with abundant methanotrophic cold seep fauna at the Central Seep location on the northern off-axis flanking regions, show consistent geochemical and microbial differences between hot, temperate, cold seep, and background sites. The changing microbial actors include autotrophic and heterotrophic bacterial and archaeal lineages that catalyze sulfur, nitrogen, and methane cycling, organic matter degradation, and hydrocarbon oxidation. Thermal, biogeochemical, and microbiological characteristics of the sampling locations indicate that sediment thermal regime and seep-derived or hydrothermal energy sources structure the microbial communities at the sediment surface.
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ArticleMicrobial community dynamics and coexistence in a sulfide-driven phototrophic bloom(Wiley, 2020-01-17) Bhatnagar, Srijak ; Cowley, Elise S. ; Kopf, Sebastian H. ; Pérez Castro, Sherlynette ; Kearney, Sean ; Dawson, Scott C. ; Hanselmann, Kurt ; Ruff, S. EmilBackground: 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.
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ArticleHydrocarbon seepage in the deep seabed links subsurface and seafloor biospheres(National Academy of Sciences, 2020-04-30) Chakraborty, Anirban ; Ruff, S. Emil ; Dong, Xiyang ; Ellefson, Emily D. ; Li, Carmen ; Brooks, James M. ; McBee, Jayme ; Bernard, Bernie B. ; Hubert, Casey R. J.Marine cold seeps transmit fluids between the subseafloor and seafloor biospheres through upward migration of hydrocarbons that originate in deep sediment layers. It remains unclear how geofluids influence the composition of the seabed microbiome and if they transport deep subsurface life up to the surface. Here we analyzed 172 marine surficial sediments from the deep-water Eastern Gulf of Mexico to assess whether hydrocarbon fluid migration is a mechanism for upward microbial dispersal. While 132 of these sediments contained migrated liquid hydrocarbons, evidence of continuous advective transport of thermogenic alkane gases was observed in 11 sediments. Gas seeps harbored distinct microbial communities featuring bacteria and archaea that are well-known inhabitants of deep biosphere sediments. Specifically, 25 distinct sequence variants within the uncultivated bacterial phyla Atribacteria and Aminicenantes and the archaeal order Thermoprofundales occurred in significantly greater relative sequence abundance along with well-known seep-colonizing members of the bacterial genus Sulfurovum, in the gas-positive sediments. Metabolic predictions guided by metagenome-assembled genomes suggested these organisms are anaerobic heterotrophs capable of nonrespiratory breakdown of organic matter, likely enabling them to inhabit energy-limited deep subseafloor ecosystems. These results point to petroleum geofluids as a vector for the advection-assisted upward dispersal of deep biosphere microbes from subsurface to surface environments, shaping the microbiome of cold seep sediments and providing a general mechanism for the maintenance of microbial diversity in the deep sea.
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ArticleDegradation of biological macromolecules supports uncultured microbial populations in Guaymas Basin hydrothermal sediments(Springer Nature, 2021-06-10) Pérez Castro, Sherlynette ; Borton, Mikayla A. ; Regan, Kathleen M. ; Hrabe de Angelis, Isabella ; Wrighton, Kelly C. ; Teske, Andreas P. ; Strous, Marc ; Ruff, S. EmilHydrothermal sediments contain large numbers of uncultured heterotrophic microbial lineages. Here, we amended Guaymas Basin sediments with proteins, polysaccharides, nucleic acids or lipids under different redox conditions and cultivated heterotrophic thermophiles with the genomic potential for macromolecule degradation. We reconstructed 20 metagenome-assembled genomes (MAGs) of uncultured lineages affiliating with known archaeal and bacterial phyla, including endospore-forming Bacilli and candidate phylum Marinisomatota. One Marinisomatota MAG had 35 different glycoside hydrolases often in multiple copies, seven extracellular CAZymes, six polysaccharide lyases, and multiple sugar transporters. This population has the potential to degrade a broad spectrum of polysaccharides including chitin, cellulose, pectin, alginate, chondroitin, and carrageenan. We also describe thermophiles affiliating with the genera Thermosyntropha, Thermovirga, and Kosmotoga with the capability to make a living on nucleic acids, lipids, or multiple macromolecule classes, respectively. Several populations seemed to lack extracellular enzyme machinery and thus likely scavenged oligo- or monomers (e.g., MAGs affiliating with Archaeoglobus) or metabolic products like hydrogen (e.g., MAGs affiliating with Thermodesulfobacterium or Desulforudaceae). The growth of methanogens or the production of methane was not observed in any condition, indicating that the tested macromolecules are not degraded into substrates for methanogenesis in hydrothermal sediments. We provide new insights into the niches, and genomes of microorganisms that actively degrade abundant necromass macromolecules under oxic, sulfate-reducing, and fermentative thermophilic conditions. These findings improve our understanding of the carbon flow across trophic levels and indicate how primary produced biomass sustains complex and productive ecosystems.
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ArticleEditorial: microbial communities and metabolisms involved in the degradation of cellular and extracellular organic biopolymers(Frontiers Media, 2022-01-04) Ruff, S. EmilMost organic matter on Earth occurs in the form of macromolecules and complex biopolymers, which include the building blocks of every organism. Plant, animal, fungal, and microbial cells largely consist of macromolecules belonging to four compound classes: proteins, polysaccharides, nucleic acids, and lipids (Figure 1). The percentage of these compounds per dry weight can vary greatly between lineages, but also between individuals of the same species or developmental stages of the same organism. Living and lysing cells release a substantial quantity and variety of macromolecules to the environment. These compounds often contain nitrogen, phosphorus, and sulfur, in addition to carbon, and are thus ideal food sources for heterotrophic organisms. Although the degradation of biopolymers and macromolecules has received considerable attention, many knowledge gaps remain, particularly in very complex ecosystems such as soils and sediments.
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ArticleCommon environmental pollutants negatively affect development and regeneration in the sea anemone Nematostella vectensis holobiont(Frontiers Media, 2021-12-23) Klein, Sylvia ; Frazier, Victoria ; Readdean, Timothy ; Lucas, Emily ; Diaz-Jimenez, Erica P. ; Sogin, Mitchell L. ; Ruff, S. Emil ; Echeverri, KarenThe anthozoan sea anemone Nematostella vectensis belongs to the phylum of cnidarians which also includes jellyfish and corals. Nematostella are native to United States East Coast marsh lands, where they constantly adapt to changes in salinity, temperature, oxygen concentration and pH. Its natural ability to continually acclimate to changing environments coupled with its genetic tractability render Nematostella a powerful model organism in which to study the effects of common pollutants on the natural development of these animals. Potassium nitrate, commonly used in fertilizers, and Phthalates, a component of plastics are frequent environmental stressors found in coastal and marsh waters. Here we present data showing how early exposure to these pollutants lead to dramatic defects in development of the embryos and eventual mortality possibly due to defects in feeding ability. Additionally, we examined the microbiome of the animals and identified shifts in the microbial community that correlated with the type of water that was used to grow the animals, and with their exposure to pollutants.
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ArticleMethane oxidation and methylotroph population dynamics in groundwater mesocosms(Wiley, 2020-02-03) Kuloyo, Olukayode ; Ruff, S. Emil ; Cahill, Aaron ; Connors, Liam ; Zorz, Jackie K. ; Hrabe de Angelis, Isabella ; Nightingale, Michael ; Mayer, Bernhard ; Strous, MarcExtraction of natural gas from unconventional hydrocarbon reservoirs by hydraulic fracturing raises concerns about methane migration into groundwater. Microbial methane oxidation can be a significant methane sink. Here, we inoculated replicated, sand‐packed, continuous mesocosms with groundwater from a field methane release experiment. The mesocosms experienced thirty‐five weeks of dynamic methane, oxygen and nitrate concentrations. We determined concentrations and stable isotope signatures of methane, carbon dioxide and nitrate and monitored microbial community composition of suspended and attached biomass. Methane oxidation was strictly dependent on oxygen availability and led to enrichment of 13C in residual methane. Nitrate did not enhance methane oxidation under oxygen limitation. Methylotrophs persisted for weeks in the absence of methane, making them a powerful marker for active as well as past methane leaks. Thirty‐nine distinct populations of methylotrophic bacteria were observed. Methylotrophs mainly occurred attached to sediment particles. Abundances of methanotrophs and other methylotrophs were roughly similar across all samples, pointing at transfer of metabolites from the former to the latter. Two populations of Gracilibacteria (Candidate Phyla Radiation) displayed successive blooms, potentially triggered by a period of methane famine. This study will guide interpretation of future field studies and provides increased understanding of methylotroph ecophysiology.