scholarly journals Genomic Evidence for Formate Metabolism by Chloroflexi as the Key to Unlocking Deep Carbon in Lost City Microbial Ecosystems

2019 ◽  
Author(s):  
Julia M. McGonigle ◽  
Susan Q. Lang ◽  
William J. Brazelton
Keyword(s):  
Carbon Cycling ◽  
Hydrothermal Vents ◽  
Reducing Power ◽  
Single Species ◽  
Hydrogen Gas ◽  
Ambient Seawater ◽  
Lost City ◽  
Microbial Life ◽  
Microbial Ecosystems ◽  
Lost City Hydrothermal Field

ABSTRACTThe Lost City hydrothermal field on the Mid-Atlantic Ridge supports dense microbial life on the lofty calcium carbonate chimney structures. The vent field is fueled by chemical reactions between the ultramafic rock under the chimneys and ambient seawater. These serpentinization reactions provide reducing power (as hydrogen gas) and organic compounds that can serve as microbial food; the most abundant of these are methane and formate. Previous studies have characterized the interior of the chimneys as a single-species biofilm inhabited by the Lost City Methanosarcinales, but also indicated that this methanogen is unable to metabolize formate. The new metagenomic results presented here indicate that carbon cycling in these Lost City chimney biofilms could depend on the metabolism of formate by low-abundance Chloroflexi species. Additionally, we present evidence that metabolically diverse, formate-utilizing Sulfurovum species are living in the transition zone between the interior and exterior of the chimneys.IMPORTANCEPrimitive forms of life may have originated around hydrothermal vents at the bottom of the ancient ocean. The Lost City hydrothermal vent field, fueled by just rock and water, provides an analog for not only primitive ecosystems but also extraterrestrial ecosystems that might support life. The microscopic life covering towering chimney structures at the Lost City has been well characterized, yet little is known about the carbon cycling in this ecosystem. These results provide a better understanding of how carbon from the deep subsurface can fuel rich microbial ecosystems on the seafloor.

scholarly journals Genomic Evidence for Formate Metabolism by Chloroflexi as the Key to Unlocking Deep Carbon in Lost City Microbial Ecosystems

2020 ◽  
Vol 86 (8) ◽  
Author(s):  
Julia M. McGonigle ◽  
Susan Q. Lang ◽  
William J. Brazelton
Keyword(s):  
Carbon Cycling ◽  
Hydrothermal Vents ◽  
Reducing Power ◽  
Single Species ◽  
Hydrogen Gas ◽  
Ambient Seawater ◽  
Lost City ◽  
Microbial Life ◽  
Microbial Ecosystems ◽  
Lost City Hydrothermal Field

ABSTRACT The Lost City hydrothermal field on the Mid-Atlantic Ridge supports dense microbial life on the lofty calcium carbonate chimney structures. The vent field is fueled by chemical reactions between the ultramafic rock under the chimneys and ambient seawater. These serpentinization reactions provide reducing power (as hydrogen gas) and organic compounds that can serve as microbial food; the most abundant of these are methane and formate. Previous studies have characterized the interior of the chimneys as a single-species biofilm inhabited by the Lost City Methanosarcinales, but they also indicated that this methanogen is unable to metabolize formate. The new metagenomic results presented here indicate that carbon cycling in these Lost City chimney biofilms could depend on the metabolism of formate by Chloroflexi populations. Additionally, we present evidence for metabolically diverse, formate-utilizing Sulfurovum populations and new genomic and phylogenetic insights into the unique Lost City Methanosarcinales. IMPORTANCE Primitive forms of life may have originated around hydrothermal vents at the bottom of the ancient ocean. The Lost City hydrothermal vent field, fueled by just rock and water, provides an analog for not only primitive ecosystems but also potential extraterrestrial rock-powered ecosystems. The microscopic life covering the towering chimney structures at the Lost City has been previously documented, yet little is known about the carbon cycling in this ecosystem. These results provide a better understanding of how carbon from the deep subsurface can fuel rich microbial ecosystems on the seafloor.

scholarly journals Habitability of the marine serpentinite subsurface: a case study of the Lost City hydrothermal field

2020 ◽  
Vol 378 (2165) ◽  
pp. 20180429 ◽  
Author(s):  
Susan Q. Lang ◽  
William J. Brazelton
Keyword(s):  
Hydrogen Gas ◽  
Hydrothermal Field ◽  
Lost City ◽  
Microbial Life ◽  
Subsurface Environments ◽  
Biological Potential ◽  
Atlantis Massif ◽  
Geochemical Reactions ◽  
Lost City Hydrothermal Field

The Lost City hydrothermal field is a dramatic example of the biological potential of serpentinization. Microbial life is prevalent throughout the Lost City chimneys, powered by the hydrogen gas and organic molecules produced by serpentinization and its associated geochemical reactions. Microbial life in the serpentinite subsurface below the Lost City chimneys, however, is unlikely to be as dense or active. The marine serpentinite subsurface poses serious challenges for microbial activity, including low porosities, the combination of stressors of elevated temperature, high pH and a lack of bioavailable ∑CO 2 . A better understanding of the biological opportunities and challenges in serpentinizing systems would provide important insights into the total habitable volume of Earth's crust and for the potential of the origin and persistence of life in Earth's subsurface environments. Furthermore, the limitations to life in serpentinizing subsurface environments on Earth have significant implications for the habitability of subsurface environments on ocean worlds such as Europa and Enceladus. Here, we review the requirements and limitations of life in serpentinizing systems, informed by our research at the Lost City and the underwater mountain on which it resides, the Atlantis Massif. This article is part of a discussion meeting issue ‘Serpentinite in the Earth System’.

scholarly journals Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization

mBio ◽  
2011 ◽  
Vol 2 (4) ◽  
Author(s):  
William J. Brazelton ◽  
Mausmi P. Mehta ◽  
Deborah S. Kelley ◽  
John A. Baross
Keyword(s):  
Methane Production ◽  
Single Species ◽  
Hydrothermal Systems ◽  
Hydrothermal Field ◽  
Metagenomic Data ◽  
Lost City ◽  
Ecological Diversification ◽  
Microbial Biofilms ◽  
Wide Range ◽  
Lost City Hydrothermal Field

ABSTRACTCarbonate chimneys at the Lost City hydrothermal field are coated in biofilms dominated by a single phylotype of archaea known as Lost CityMethanosarcinales. In this study, we have detected surprising physiological complexity in single-species biofilms, which is typically indicative of multispecies biofilm communities. Multiple cell morphologies were visible within the biofilms by transmission electron microscopy, and some cells contained intracellular membranes that may facilitate methane oxidation. Both methane production and oxidation were detected at 70 to 80°C and pH 9 to 10 in samples containing the single-species biofilms. Both processes were stimulated by the presence of hydrogen (H2), indicating that methane production and oxidation are part of a syntrophic interaction. Metagenomic data included a sequence encoding AMP-forming acetyl coenzyme A synthetase, indicating that acetate may play a role in the methane-cycling syntrophy. A wide range of nitrogen fixation genes were also identified, many of which were likely acquired via lateral gene transfer (LGT). Our results indicate that cells within these single-species biofilms may have differentiated into multiple physiological roles to form multicellular communities linked by metabolic interactions and LGT. Communities similar to these Lost City biofilms are likely to have existed early in the evolution of life, and we discuss how the multicellular characteristics of ancient hydrogen-fueled biofilm communities could have stimulated ecological diversification, as well as unity of biochemistry, during the earliest stages of cellular evolution.IMPORTANCEOur previous work at the Lost City hydrothermal field has shown that its carbonate chimneys host microbial biofilms dominated by a single uncultivated “species” of archaea. In this paper, we integrate evidence from these previous studies with new data on the metabolic activity and cellular morphology of these archaeal biofilms. We conclude that the archaeal biofilm must contain cells that are physiologically and possibly genetically differentiated with respect to each other. These results are especially interesting considering the possibility that the first cells originated and evolved in hydrothermal systems similar to Lost City.

scholarly journals Bacterial Communities Associated with Subsurface Geochemical Processes in Continental Serpentinite Springs

2013 ◽  
Vol 79 (13) ◽  
pp. 3906-3916 ◽  
Author(s):  
William J. Brazelton ◽  
Penny L. Morrill ◽  
Natalie Szponar ◽  
Matthew O. Schrenk
Keyword(s):  
Hydrothermal Vents ◽  
Interdisciplinary Approach ◽  
Rrna Gene ◽  
Molecular Fingerprinting ◽  
Near Surface ◽  
Content Type ◽  
Lost City ◽  
Biogeographic Pattern ◽  
Geochemical Factors ◽  
Lost City Hydrothermal Field

ABSTRACTReactions associated with the geochemical process of serpentinization can generate copious quantities of hydrogen and low-molecular-weight organic carbon compounds, which may provide energy and nutrients to sustain subsurface microbial communities independently of the photosynthetically supported surface biosphere. Previous microbial ecology studies have tested this hypothesis in deep sea hydrothermal vents, such as the Lost City hydrothermal field. This study applied similar methods, including molecular fingerprinting and tag sequencing of the 16S rRNA gene, to ultrabasic continental springs emanating from serpentinizing ultramafic rocks. These molecular surveys were linked with geochemical measurements of the fluids in an interdisciplinary approach designed to distinguish potential subsurface organisms from those derived from surface habitats. The betaproteobacterial genusHydrogenophagawas identified as a likely inhabitant of transition zones where hydrogen-enriched subsurface fluids mix with oxygenated surface water. TheFirmicutesgenusErysipelothrixwas most strongly correlated with geochemical factors indicative of subsurface fluids and was identified as the most likely inhabitant of a serpentinization-powered subsurface biosphere. Both of these taxa have been identified in multiple hydrogen-enriched subsurface habitats worldwide, and the results of this study contribute to an emerging biogeographic pattern in whichBetaproteobacteriaoccur in near-surface mixing zones andFirmicutesare present in deeper, anoxic subsurface habitats.

An Ordovician “Lost City” — venting serpentinite and life oases on Iapetus seafloor

2010 ◽  
Vol 47 (3) ◽  
pp. 199-207 ◽  
Author(s):  
Denis Lavoie ◽  
Guoxiang Chi
Keyword(s):  
Biological Activity ◽  
High Temperature ◽  
Low Temperature ◽  
Open System ◽  
Isotopic Fractionation ◽  
Marine Waters ◽  
Lost City ◽  
Microbial Life ◽  
Carbonate Cements ◽  
Lost City Hydrothermal Field

Highly brecciated carbonate-rich serpentinites (or ophicalcites) of Early Ordovician age in the Dunnage Zone of Quebec are host to fracture-fill, high-temperature (80–230 °C) carbonate cements. Away from, or crosscut by the fractures, centimetre- to decimetre-thick crusts made up of massive to laminated micrite, peloidal layers and threads are associated with low-temperature botryoidal calcite cements. The peloidal masses are characterized by a clotted texture that is reminiscent of interpreted fossilized Ordovician microbial communities. The ophicalcite contains carbonate botryoids, morphology commonly found at shallow reefal margins but also at modern cold CH4 seeps and recently documented at hot CH4 vents from serpentinite, such as the modern Lost City hydrothermal field in the Atlantic Ocean. The δ18OVPDB ratios of the calcite botryoids and peloidal layers indicate formation and (or) precipitation out of cold Ordovician deep-marine waters. To the contrary of botryoids at cold methane seeps, the botryoids associated with the modern and Ordovician hot vents do not show the negative δ13CVPDB ratios indicative of microbial isotopic fractionation. Therefore, any microbial-derived HCO3– has been overwhelmed by the isotopically heavier marine-derived carbon during the open-system diagenesis. Carbonate-rich serpentinites should be carefully revisited in the search for evidence of microbial life in the Precambrian, as the negative δ13CVPDB ratios used as fingerprints of biological activity are not always reliable.

scholarly journals Ultra-small cells and DPANN genome unveiled inside an extinct vent chimney

2021 ◽  
Author(s):  
Hinako Takamiya ◽  
Mariko Kouduka ◽  
Hitoshi Furutani ◽  
Hiroki Mukai ◽  
Takushi Yamamoto ◽  
...  
Keyword(s):  
Nucleic Acids ◽  
Grain Boundaries ◽  
Deep Sea ◽  
Hydrothermal Vents ◽  
Single Gene ◽  
Metal Sulfide ◽  
Small Cells ◽  
Acid Fermentation ◽  
Microbial Life ◽  
Fluid Venting

AbstractChemosynthetic organisms flourish around deep-sea hydrothermal vents where energy-rich fluids are emitted from metal sulfide chimneys. In contrast to actively venting chimneys, the nature of microbial life in extinct chimneys without fluid venting remains largely unknown. Here, the occurrence of ultra-small cells in silica-filled grain boundaries inside an extinct chimney is demonstrated by high-resolution bio-signature mapping. The ultra-small cells are associated with extracellularly precipitated Cu2O nanocrystals. Single-gene analysis shows that the chimney interior is dominated by a member of Pacearchaeota known as a major phylum of DPANN. Genome-resolved metagenomic analysis reveals that the chimney Pacearchaeota member is equipped with a nearly full set of genes for fermentation-based energy generation from nucleic acids, in contrast to previously characterized Pacearchaeota members lacking many genes for nucleic acid fermentation. We infer that the ultra-small cells associated with silica and extracellular Cu2O nanocrystals in the grain boundaries are Pacearchaeota, on the basis of the experimentally demonstrated capability of silica to concentrate nucleic acids from seawater and the presence of Cu-exporting genes in a reconstructed Pacearchaeota genome. Given the existence of ~3-billion-year-old submarine hydrothermally deposited silica, proliferation of microbial life using silica-bound nucleic acids might be relevant to the primitive vent biosphere.

scholarly journals Prospects for metazoan life in sub-glacial Antarctic lakes: the most extreme life on Earth?

2019 ◽  
Vol 18 (05) ◽  
pp. 416-419 ◽  
Author(s):  
Sven Thatje ◽  
Alastair Brown ◽  
Claus-Dieter Hillenbrand
Keyword(s):  
Hydrothermal Vents ◽  
Pure Water ◽  
Hydrothermal Activity ◽  
Microbial Life ◽  
Lake Vostok ◽  
Physico Chemical ◽  
Physiological Adaptations ◽  
Subglacial Lakes ◽  
Life On Earth ◽  
Harsh Conditions

AbstractAbout 400 subglacial lakes are known from Antarctica. The question of whether life unique of subglacial lakes exists has been paramount since their discovery. Despite frequent evidence of microbial life mostly from accretion ice, subglacial lakes are characterized by physiologically hostile conditions to metazoan life, as we know it. Pure water (salinity ≤0.4–1.2%), extreme cold (−3°C), high hydrostatic pressure, areas of limited or no oxygen availability and permanent darkness altogether require physiological adaptations to these harsh conditions. The record of gene sequences including some associated with hydrothermal vents does foster the idea of metazoan life in Lake Vostok. Here, we synthesize the physico-chemical environment surrounding sub-glacial lakes and potential sites of hydrothermal activity and advocate that the physico-chemical stability found at these sites may be the most likely sites for metazoan life to exist. The unique conditions presented by Lake Vostok may also offer an outlook on life to be expected in extra-terrestrial subglacial environments, such as on Jupiter's moon Europa or Saturn's moon Enceladus.

Organic complexation of copper in deep-sea hydrothermal vent systems

2007 ◽  
Vol 4 (2) ◽  
pp. 81 ◽  
Author(s):  
Sylvia G. Sander ◽  
Andrea Koschinsky ◽  
Gary Massoth ◽  
Matthew Stott ◽  
Keith A. Hunter
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vent ◽  
Hydrothermal Vents ◽  
Natural Habitat ◽  
Hydrothermal Systems ◽  
Conditional Stability ◽  
Copper Binding ◽  
Medium Temperature ◽  
Ambient Seawater ◽  
Organic Complexation

Environmental context. Deep-sea hydrothermal vents represent a natural habitat for many extremophile organisms able to cope with extreme physical and chemical conditions, including high loads of heavy metals and reduced gases. To date, no information is available on the level and role of organic complexation of metals in these systems, which will have consequences on the bioavailability and precipitation or mineralisation of metals. In this work, we give evidence for the presence of organic molecules, including thiols, capable of forming complexes with copper strong enough to compete against sulfide present at high levels in hydrothermal systems. Abstract. Here we report, for the first time, that strong organic complexation plays an important role in the chemical speciation of copper in hydrothermal vent systems including medium temperature outlets, diffuse vents with an adjacent hydrothermal biocommunity, and local mixing zone with seawater. Samples from three deep-sea hydrothermal vent areas show a wide concentration range of organic copper-binding ligands, up to 4000 nM, with very high conditional stability constants (log K′Cu′L = 12.48 to 13.46). Measurements were usually made using voltammetric methods after removal of sulfide species under ambient seawater conditions (pH 7.8), but binding still occurs at pH 4.5 and 2.1. The voltammetric behaviour of our hydrothermal samples is compared with that of glutathione (GSH) a known strong Cu-binding ligand, as a representative of an organic thiol. Our results provide compelling evidence for the presence of organic ligands, including thiols, which form complexes strong enough to play an important role in controlling the bioavailability and geochemical behaviour of metal ions around hydrothermal vents.

scholarly journals Geologic evolution of the Lost City Hydrothermal Field

2016 ◽  
Vol 17 (2) ◽  
pp. 375-394 ◽  
Author(s):  
Alden R. Denny ◽  
Deborah S. Kelley ◽  
Gretchen L. Früh-Green
Keyword(s):  
Hydrothermal Field ◽  
Lost City ◽  
Lost City Hydrothermal Field
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