Potential role for microbial ureolysis in the rapid formation of carbonate tufa mounds

Fernando Medina Ferrer; Michael R. Rosen; Jayme Feyhl-Buska; Virginia V. Russell; Fredrik Sønderholm; Sean Loyd; Russell Shapiro; Blake W. Stamps; Victoria Petryshyn; Cansu Demirel-Floyd; Jake V. Bailey; Hope A. Johnson; John R. Spear; Frank A. Corsetti

doi:10.1111/gbi.12467

Potential role for microbial ureolysis in the rapid formation of carbonate tufa mounds

Fernando Medina Ferrer, Michael R. Rosen, Jayme Feyhl-Buska, Virginia V. Russell, Fredrik Sønderholm, Sean Loyd, Russell Shapiro, Blake W. Stamps, Victoria Petryshyn, Cansu Demirel-Floyd, Jake V. Bailey, Hope A. Johnson, John R. Spear, Frank A. Corsetti

Earth and Environmental Sciences-Twin Cities

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

Modern carbonate tufa towers in the alkaline (~pH 9.5) Big Soda Lake (BSL), Nevada, exhibit rapid precipitation rates (exceeding 3 cm/year) and host diverse microbial communities. Geochemical indicators reveal that carbonate precipitation is, in part, promoted by the mixing of calcium-rich groundwater and carbonate-rich lake water, such that a microbial role for carbonate precipitation is unknown. Here, we characterize the BSL microbial communities and evaluate their potential effects on carbonate precipitation that may influence fast carbonate precipitation rates of the active tufa mounds of BSL. Small subunit rRNA gene surveys indicate a diverse microbial community living endolithically, in interior voids, and on tufa surfaces. Metagenomic DNA sequencing shows that genes associated with metabolisms that are capable of increasing carbonate saturation (e.g., photosynthesis, ureolysis, and bicarbonate transport) are abundant. Enzyme activity assays revealed that urease and carbonic anhydrase, two microbial enzymes that promote carbonate precipitation, are active in situ in BSL tufa biofilms, and urease also increased calcium carbonate precipitation rates in laboratory incubation analyses. We propose that, although BSL tufas form partially as a result of water mixing, tufa-inhabiting microbiota promote rapid carbonate authigenesis via ureolysis, and potentially via bicarbonate dehydration and CO₂ outgassing by carbonic anhydrase. Microbially induced calcium carbonate precipitation in BSL tufas may generate signatures preserved in the carbonate microfabric, such as stromatolitic layers, which could serve as models for developing potential biosignatures on Earth and elsewhere.

Original language	English (US)
Pages (from-to)	79-97
Number of pages	19
Journal	Geobiology
Volume	20
Issue number	1
Early online date	Aug 2 2021
DOIs	https://doi.org/10.1111/gbi.12467
State	Published - Jan 2022

Bibliographical note

Funding Information:
We gratefully thank all students, instructors, and organizers of the 2016 International GeoBiology Course for assisting with sample collection, laboratory analysis, and discussions. This work would not have been possible without the enthusiasm and passion of Dr. Michael R. Rosen (January 19, 1961?April 27, 2021). The authors mourn his passing and will miss him as a colleague and a friend. The authors declare no conflict of interest and thank Barbara MacGregor and John Warden for helpful reviews, as well as the University of Oklahoma Supercomputing Center for Education and Research, and the Minnesota Supercomputing Institute at the University of Minnesota for archival storage and analysis resources. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This research was funded by the Agouron Institute, the Center for the Dark Energy Biosphere Investigations (C-DEBI) at the University of Southern California (USC), the USC Wrigley Institute, and NASA Exobiology grant NNX14AK20G to JVB. FMF was supported by the UMN Graduate School DDF, Fulbright 15150776, and CONICYT folio-72160214. JRS is supported by the NASA Astrobiology Rock Powered Life grant.

Funding Information:
We gratefully thank all students, instructors, and organizers of the 2016 International GeoBiology Course for assisting with sample collection, laboratory analysis, and discussions. This work would not have been possible without the enthusiasm and passion of Dr. Michael R. Rosen (January 19, 1961–April 27, 2021). The authors mourn his passing and will miss him as a colleague and a friend. The authors declare no conflict of interest and thank Barbara MacGregor and John Warden for helpful reviews, as well as the University of Oklahoma Supercomputing Center for Education and Research, and the Minnesota Supercomputing Institute at the University of Minnesota for archival storage and analysis resources. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This research was funded by the Agouron Institute, the Center for the Dark Energy Biosphere Investigations (C‐DEBI) at the University of Southern California (USC), the USC Wrigley Institute, and NASA Exobiology grant NNX14AK20G to JVB. FMF was supported by the UMN Graduate School DDF, Fulbright 15150776, and CONICYT folio‐72160214. JRS is supported by the NASA Astrobiology Rock Powered Life grant.

Publisher Copyright:
© 2021 John Wiley & Sons Ltd.

Keywords

Big Soda Lake
MICP
carbonic anhydrase
microbialite
tufa tower
urease

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10.1111/gbi.12467

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Medina Ferrer, F., Rosen, M. R., Feyhl-Buska, J., Russell, V. V., Sønderholm, F., Loyd, S., Shapiro, R., Stamps, B. W., Petryshyn, V., Demirel-Floyd, C., Bailey, J. V., Johnson, H. A., Spear, J. R., & Corsetti, F. A. (2022). Potential role for microbial ureolysis in the rapid formation of carbonate tufa mounds. Geobiology, 20(1), 79-97. https://doi.org/10.1111/gbi.12467

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title = "Potential role for microbial ureolysis in the rapid formation of carbonate tufa mounds",

abstract = "Modern carbonate tufa towers in the alkaline (~pH 9.5) Big Soda Lake (BSL), Nevada, exhibit rapid precipitation rates (exceeding 3 cm/year) and host diverse microbial communities. Geochemical indicators reveal that carbonate precipitation is, in part, promoted by the mixing of calcium-rich groundwater and carbonate-rich lake water, such that a microbial role for carbonate precipitation is unknown. Here, we characterize the BSL microbial communities and evaluate their potential effects on carbonate precipitation that may influence fast carbonate precipitation rates of the active tufa mounds of BSL. Small subunit rRNA gene surveys indicate a diverse microbial community living endolithically, in interior voids, and on tufa surfaces. Metagenomic DNA sequencing shows that genes associated with metabolisms that are capable of increasing carbonate saturation (e.g., photosynthesis, ureolysis, and bicarbonate transport) are abundant. Enzyme activity assays revealed that urease and carbonic anhydrase, two microbial enzymes that promote carbonate precipitation, are active in situ in BSL tufa biofilms, and urease also increased calcium carbonate precipitation rates in laboratory incubation analyses. We propose that, although BSL tufas form partially as a result of water mixing, tufa-inhabiting microbiota promote rapid carbonate authigenesis via ureolysis, and potentially via bicarbonate dehydration and CO2 outgassing by carbonic anhydrase. Microbially induced calcium carbonate precipitation in BSL tufas may generate signatures preserved in the carbonate microfabric, such as stromatolitic layers, which could serve as models for developing potential biosignatures on Earth and elsewhere.",

keywords = "Big Soda Lake, MICP, carbonic anhydrase, microbialite, tufa tower, urease",

author = "{Medina Ferrer}, Fernando and Rosen, {Michael R.} and Jayme Feyhl-Buska and Russell, {Virginia V.} and Fredrik S{\o}nderholm and Sean Loyd and Russell Shapiro and Stamps, {Blake W.} and Victoria Petryshyn and Cansu Demirel-Floyd and Bailey, {Jake V.} and Johnson, {Hope A.} and Spear, {John R.} and Corsetti, {Frank A.}",

note = "Funding Information: We gratefully thank all students, instructors, and organizers of the 2016 International GeoBiology Course for assisting with sample collection, laboratory analysis, and discussions. This work would not have been possible without the enthusiasm and passion of Dr. Michael R. Rosen (January 19, 1961?April 27, 2021). The authors mourn his passing and will miss him as a colleague and a friend. The authors declare no conflict of interest and thank Barbara MacGregor and John Warden for helpful reviews, as well as the University of Oklahoma Supercomputing Center for Education and Research, and the Minnesota Supercomputing Institute at the University of Minnesota for archival storage and analysis resources. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This research was funded by the Agouron Institute, the Center for the Dark Energy Biosphere Investigations (C-DEBI) at the University of Southern California (USC), the USC Wrigley Institute, and NASA Exobiology grant NNX14AK20G to JVB. FMF was supported by the UMN Graduate School DDF, Fulbright 15150776, and CONICYT folio-72160214. JRS is supported by the NASA Astrobiology Rock Powered Life grant. Funding Information: We gratefully thank all students, instructors, and organizers of the 2016 International GeoBiology Course for assisting with sample collection, laboratory analysis, and discussions. This work would not have been possible without the enthusiasm and passion of Dr. Michael R. Rosen (January 19, 1961–April 27, 2021). The authors mourn his passing and will miss him as a colleague and a friend. The authors declare no conflict of interest and thank Barbara MacGregor and John Warden for helpful reviews, as well as the University of Oklahoma Supercomputing Center for Education and Research, and the Minnesota Supercomputing Institute at the University of Minnesota for archival storage and analysis resources. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This research was funded by the Agouron Institute, the Center for the Dark Energy Biosphere Investigations (C‐DEBI) at the University of Southern California (USC), the USC Wrigley Institute, and NASA Exobiology grant NNX14AK20G to JVB. FMF was supported by the UMN Graduate School DDF, Fulbright 15150776, and CONICYT folio‐72160214. JRS is supported by the NASA Astrobiology Rock Powered Life grant. Publisher Copyright: {\textcopyright} 2021 John Wiley & Sons Ltd.",

year = "2022",

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doi = "10.1111/gbi.12467",

language = "English (US)",

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T1 - Potential role for microbial ureolysis in the rapid formation of carbonate tufa mounds

AU - Medina Ferrer, Fernando

AU - Rosen, Michael R.

AU - Feyhl-Buska, Jayme

AU - Russell, Virginia V.

AU - Sønderholm, Fredrik

AU - Loyd, Sean

AU - Shapiro, Russell

AU - Stamps, Blake W.

AU - Petryshyn, Victoria

AU - Demirel-Floyd, Cansu

AU - Bailey, Jake V.

AU - Johnson, Hope A.

AU - Spear, John R.

AU - Corsetti, Frank A.

N1 - Funding Information: We gratefully thank all students, instructors, and organizers of the 2016 International GeoBiology Course for assisting with sample collection, laboratory analysis, and discussions. This work would not have been possible without the enthusiasm and passion of Dr. Michael R. Rosen (January 19, 1961?April 27, 2021). The authors mourn his passing and will miss him as a colleague and a friend. The authors declare no conflict of interest and thank Barbara MacGregor and John Warden for helpful reviews, as well as the University of Oklahoma Supercomputing Center for Education and Research, and the Minnesota Supercomputing Institute at the University of Minnesota for archival storage and analysis resources. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This research was funded by the Agouron Institute, the Center for the Dark Energy Biosphere Investigations (C-DEBI) at the University of Southern California (USC), the USC Wrigley Institute, and NASA Exobiology grant NNX14AK20G to JVB. FMF was supported by the UMN Graduate School DDF, Fulbright 15150776, and CONICYT folio-72160214. JRS is supported by the NASA Astrobiology Rock Powered Life grant. Funding Information: We gratefully thank all students, instructors, and organizers of the 2016 International GeoBiology Course for assisting with sample collection, laboratory analysis, and discussions. This work would not have been possible without the enthusiasm and passion of Dr. Michael R. Rosen (January 19, 1961–April 27, 2021). The authors mourn his passing and will miss him as a colleague and a friend. The authors declare no conflict of interest and thank Barbara MacGregor and John Warden for helpful reviews, as well as the University of Oklahoma Supercomputing Center for Education and Research, and the Minnesota Supercomputing Institute at the University of Minnesota for archival storage and analysis resources. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This research was funded by the Agouron Institute, the Center for the Dark Energy Biosphere Investigations (C‐DEBI) at the University of Southern California (USC), the USC Wrigley Institute, and NASA Exobiology grant NNX14AK20G to JVB. FMF was supported by the UMN Graduate School DDF, Fulbright 15150776, and CONICYT folio‐72160214. JRS is supported by the NASA Astrobiology Rock Powered Life grant. Publisher Copyright: © 2021 John Wiley & Sons Ltd.

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N2 - Modern carbonate tufa towers in the alkaline (~pH 9.5) Big Soda Lake (BSL), Nevada, exhibit rapid precipitation rates (exceeding 3 cm/year) and host diverse microbial communities. Geochemical indicators reveal that carbonate precipitation is, in part, promoted by the mixing of calcium-rich groundwater and carbonate-rich lake water, such that a microbial role for carbonate precipitation is unknown. Here, we characterize the BSL microbial communities and evaluate their potential effects on carbonate precipitation that may influence fast carbonate precipitation rates of the active tufa mounds of BSL. Small subunit rRNA gene surveys indicate a diverse microbial community living endolithically, in interior voids, and on tufa surfaces. Metagenomic DNA sequencing shows that genes associated with metabolisms that are capable of increasing carbonate saturation (e.g., photosynthesis, ureolysis, and bicarbonate transport) are abundant. Enzyme activity assays revealed that urease and carbonic anhydrase, two microbial enzymes that promote carbonate precipitation, are active in situ in BSL tufa biofilms, and urease also increased calcium carbonate precipitation rates in laboratory incubation analyses. We propose that, although BSL tufas form partially as a result of water mixing, tufa-inhabiting microbiota promote rapid carbonate authigenesis via ureolysis, and potentially via bicarbonate dehydration and CO2 outgassing by carbonic anhydrase. Microbially induced calcium carbonate precipitation in BSL tufas may generate signatures preserved in the carbonate microfabric, such as stromatolitic layers, which could serve as models for developing potential biosignatures on Earth and elsewhere.

AB - Modern carbonate tufa towers in the alkaline (~pH 9.5) Big Soda Lake (BSL), Nevada, exhibit rapid precipitation rates (exceeding 3 cm/year) and host diverse microbial communities. Geochemical indicators reveal that carbonate precipitation is, in part, promoted by the mixing of calcium-rich groundwater and carbonate-rich lake water, such that a microbial role for carbonate precipitation is unknown. Here, we characterize the BSL microbial communities and evaluate their potential effects on carbonate precipitation that may influence fast carbonate precipitation rates of the active tufa mounds of BSL. Small subunit rRNA gene surveys indicate a diverse microbial community living endolithically, in interior voids, and on tufa surfaces. Metagenomic DNA sequencing shows that genes associated with metabolisms that are capable of increasing carbonate saturation (e.g., photosynthesis, ureolysis, and bicarbonate transport) are abundant. Enzyme activity assays revealed that urease and carbonic anhydrase, two microbial enzymes that promote carbonate precipitation, are active in situ in BSL tufa biofilms, and urease also increased calcium carbonate precipitation rates in laboratory incubation analyses. We propose that, although BSL tufas form partially as a result of water mixing, tufa-inhabiting microbiota promote rapid carbonate authigenesis via ureolysis, and potentially via bicarbonate dehydration and CO2 outgassing by carbonic anhydrase. Microbially induced calcium carbonate precipitation in BSL tufas may generate signatures preserved in the carbonate microfabric, such as stromatolitic layers, which could serve as models for developing potential biosignatures on Earth and elsewhere.

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Potential role for microbial ureolysis in the rapid formation of carbonate tufa mounds

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