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Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats

Dong, Yiran ; Sanford, Robert A ; Inskeep, William P ; Srivastava, Vaibhav ; Bulone, Vincent ; Fields, Christopher J ; Yau, Peter M ; Sivaguru, Mayandi ; Ahrén, Dag LU and Fouke, Kyle W , et al. (2019) In Astrobiology 19(12).
Abstract

The evolutionarily ancient Aquificales bacterium Sulfurihydrogenibium spp. dominates filamentous microbial mat communities in shallow, fast-flowing, and dysoxic hot-spring drainage systems around the world. In the present study, field observations of these fettuccini-like microbial mats at Mammoth Hot Springs in Yellowstone National Park are integrated with geology, geochemistry, hydrology, microscopy, and multi-omic molecular biology analyses. Strategic sampling of living filamentous mats along with the hot-spring CaCO3 (travertine) in which they are actively being entombed and fossilized has permitted the first direct linkage of Sulfurihydrogenibium spp. physiology and metabolism with the formation of distinct travertine streamer... (More)

The evolutionarily ancient Aquificales bacterium Sulfurihydrogenibium spp. dominates filamentous microbial mat communities in shallow, fast-flowing, and dysoxic hot-spring drainage systems around the world. In the present study, field observations of these fettuccini-like microbial mats at Mammoth Hot Springs in Yellowstone National Park are integrated with geology, geochemistry, hydrology, microscopy, and multi-omic molecular biology analyses. Strategic sampling of living filamentous mats along with the hot-spring CaCO3 (travertine) in which they are actively being entombed and fossilized has permitted the first direct linkage of Sulfurihydrogenibium spp. physiology and metabolism with the formation of distinct travertine streamer microbial biomarkers. Results indicate that, during chemoautotrophy and CO2 carbon fixation, the 87-98% Sulfurihydrogenibium-dominated mats utilize chaperons to facilitate enzyme stability and function. High-abundance transcripts and proteins for type IV pili and extracellular polymeric substances (EPSs) are consistent with their strong mucus-rich filaments tens of centimeters long that withstand hydrodynamic shear as they become encrusted by more than 5 mm of travertine per day. Their primary energy source is the oxidation of reduced sulfur (e.g., sulfide, sulfur, or thiosulfate) and the simultaneous uptake of extremely low concentrations of dissolved O2 facilitated by bd-type cytochromes. The formation of elevated travertine ridges permits the Sulfurihydrogenibium-dominated mats to create a shallow platform from which to access low levels of dissolved oxygen at the virtual exclusion of other microorganisms. These ridged travertine streamer microbial biomarkers are well preserved and create a robust fossil record of microbial physiological and metabolic activities in modern and ancient hot-spring ecosystems.

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Astrobiology
volume
19
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12
publisher
Mary Ann Liebert, Inc.
external identifiers
  • pmid:31038352
ISSN
1557-8070
DOI
10.1089/ast.2018.1965
language
English
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yes
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1468e358-c658-46a8-8c19-206f77c5ffcf
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2019-06-19 09:45:40
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2020-01-10 12:39:25
@article{1468e358-c658-46a8-8c19-206f77c5ffcf,
  abstract     = {<p>The evolutionarily ancient Aquificales bacterium Sulfurihydrogenibium spp. dominates filamentous microbial mat communities in shallow, fast-flowing, and dysoxic hot-spring drainage systems around the world. In the present study, field observations of these fettuccini-like microbial mats at Mammoth Hot Springs in Yellowstone National Park are integrated with geology, geochemistry, hydrology, microscopy, and multi-omic molecular biology analyses. Strategic sampling of living filamentous mats along with the hot-spring CaCO3 (travertine) in which they are actively being entombed and fossilized has permitted the first direct linkage of Sulfurihydrogenibium spp. physiology and metabolism with the formation of distinct travertine streamer microbial biomarkers. Results indicate that, during chemoautotrophy and CO2 carbon fixation, the 87-98% Sulfurihydrogenibium-dominated mats utilize chaperons to facilitate enzyme stability and function. High-abundance transcripts and proteins for type IV pili and extracellular polymeric substances (EPSs) are consistent with their strong mucus-rich filaments tens of centimeters long that withstand hydrodynamic shear as they become encrusted by more than 5 mm of travertine per day. Their primary energy source is the oxidation of reduced sulfur (e.g., sulfide, sulfur, or thiosulfate) and the simultaneous uptake of extremely low concentrations of dissolved O2 facilitated by bd-type cytochromes. The formation of elevated travertine ridges permits the Sulfurihydrogenibium-dominated mats to create a shallow platform from which to access low levels of dissolved oxygen at the virtual exclusion of other microorganisms. These ridged travertine streamer microbial biomarkers are well preserved and create a robust fossil record of microbial physiological and metabolic activities in modern and ancient hot-spring ecosystems.</p>},
  author       = {Dong, Yiran and Sanford, Robert A and Inskeep, William P and Srivastava, Vaibhav and Bulone, Vincent and Fields, Christopher J and Yau, Peter M and Sivaguru, Mayandi and Ahrén, Dag and Fouke, Kyle W and Weber, Joseph and Werth, Charles R and Cann, Isaac K and Keating, Kathleen M and Khetani, Radhika S and Hernandez, Alvaro G and Wright, Chris and Band, Mark and Imai, Brian S and Fried, Glenn A and Fouke, Bruce W},
  issn         = {1557-8070},
  language     = {eng},
  month        = {04},
  number       = {12},
  publisher    = {Mary Ann Liebert, Inc.},
  series       = {Astrobiology},
  title        = {Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats},
  url          = {http://dx.doi.org/10.1089/ast.2018.1965},
  doi          = {10.1089/ast.2018.1965},
  volume       = {19},
  year         = {2019},
}