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

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 H...

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Autores principales: Dong, Yiran, Sanford, Robert A., Inskeep, William P., Srivastava, Vaibhav, Bulone, Vincent, Fields, Christopher J., Yau, Peter M., Sivaguru, Mayandi, Ahrén, Dag, Fouke, Kyle W., Weber, Joseph, Werth, Charles R., Cann, Isaac K., Keating, Kathleen M., Khetani, Radhika S., Hernandez, Alvaro G., Wright, Chris, Band, Mark, Imai, Brian S., Fried, Glenn A., Fouke, Bruce W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Mary Ann Liebert, Inc., publishers 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6918859/
https://www.ncbi.nlm.nih.gov/pubmed/31038352
http://dx.doi.org/10.1089/ast.2018.1965
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author Dong, Yiran
Sanford, Robert A.
Inskeep, William P.
Srivastava, Vaibhav
Bulone, Vincent
Fields, Christopher J.
Yau, Peter M.
Sivaguru, Mayandi
Ahrén, Dag
Fouke, Kyle W.
Weber, Joseph
Werth, Charles R.
Cann, Isaac K.
Keating, Kathleen M.
Khetani, Radhika S.
Hernandez, Alvaro G.
Wright, Chris
Band, Mark
Imai, Brian S.
Fried, Glenn A.
Fouke, Bruce W.
author_facet Dong, Yiran
Sanford, Robert A.
Inskeep, William P.
Srivastava, Vaibhav
Bulone, Vincent
Fields, Christopher J.
Yau, Peter M.
Sivaguru, Mayandi
Ahrén, Dag
Fouke, Kyle W.
Weber, Joseph
Werth, Charles R.
Cann, Isaac K.
Keating, Kathleen M.
Khetani, Radhika S.
Hernandez, Alvaro G.
Wright, Chris
Band, Mark
Imai, Brian S.
Fried, Glenn A.
Fouke, Bruce W.
author_sort Dong, Yiran
collection PubMed
description 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 CaCO(3) (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 CO(2) 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 O(2) 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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spelling pubmed-69188592019-12-23 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 Fouke, Kyle W. Weber, Joseph Werth, Charles R. Cann, Isaac K. Keating, Kathleen M. Khetani, Radhika S. Hernandez, Alvaro G. Wright, Chris Band, Mark Imai, Brian S. Fried, Glenn A. Fouke, Bruce W. Astrobiology Research Articles 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 CaCO(3) (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 CO(2) 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 O(2) 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. Mary Ann Liebert, Inc., publishers 2019-12-01 2019-12-04 /pmc/articles/PMC6918859/ /pubmed/31038352 http://dx.doi.org/10.1089/ast.2018.1965 Text en © Yiran Dong et al., 2019; Published by Mary Ann Liebert, Inc. This Open Access article is distributed under the terms of the Creative Commons Attribution Noncommercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
spellingShingle Research Articles
Dong, Yiran
Sanford, Robert A.
Inskeep, William P.
Srivastava, Vaibhav
Bulone, Vincent
Fields, Christopher J.
Yau, Peter M.
Sivaguru, Mayandi
Ahrén, Dag
Fouke, Kyle W.
Weber, Joseph
Werth, Charles R.
Cann, Isaac K.
Keating, Kathleen M.
Khetani, Radhika S.
Hernandez, Alvaro G.
Wright, Chris
Band, Mark
Imai, Brian S.
Fried, Glenn A.
Fouke, Bruce W.
Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats
title Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats
title_full Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats
title_fullStr Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats
title_full_unstemmed Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats
title_short Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats
title_sort physiology, metabolism, and fossilization of hot-spring filamentous microbial mats
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6918859/
https://www.ncbi.nlm.nih.gov/pubmed/31038352
http://dx.doi.org/10.1089/ast.2018.1965
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