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Title: Active sulfur cycling in the terrestrial deep subsurface

Abstract

The deep terrestrial subsurface remains an environment where there is limited understanding of the extant microbial metabolisms. At Olkiluoto, Finland, a deep geological repository is under construction for the final storage of spent nuclear fuel. It is therefore critical to evaluate the potential impact microbial metabolism, including sulfide generation, could have upon the safety of the repository. As such, we investigated a deep groundwater where sulfate is present, but groundwater geochemistry suggests limited microbial sulfate-reducing activity. Examination of the microbial community at the genome-level revealed microorganisms with the metabolic capacity for both oxidative and reductive sulfur transformations. Deltaproteobacteria are shown to have the genetic capacity for sulfate reduction and possibly sulfur disproportionation, while Rhizobiaceae, Rhodocyclaceae, Sideroxydans, and Sulfurimonas oxidize reduced sulfur compounds. Further examination of the proteome confirmed an active sulfur cycle, serving for microbial energy generation and growth. Our results reveal that this sulfide-poor groundwater harbors an active microbial community of sulfate-reducing and sulfide-oxidizing bacteria, together mediating a sulfur cycle that remained undetected by geochemical monitoring alone. The ability of sulfide-oxidizing bacteria to limit the accumulation of sulfide was further demonstrated in groundwater incubations and highlights a potential sink for sulfide that could be beneficial for geological repository safety.

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [3];  [4]; ORCiD logo [4]; ORCiD logo [5];  [6]; ORCiD logo [6]
+ Show Author Affiliations
  1. Ecole Polytechnique Federale Lausanne (Switzlerland); Univ. of Calgary, AB (Canada)
  2. Posiva Oy, Eurajoki (Finland)
  3. KTH Royal Inst. of Technology, Stockholm (Sweden)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  5. (Bob) L. [Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  6. Ecole Polytechnique Federale Lausanne (Switzlerland)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
Posiva Oy; The Census of Deep Life within the Deep Carbon Observatory; USDOE Office of Science (SC)
OSTI Identifier:
1606636
Grant/Contract Number:  
AC05-00OR22725; 2015-06-17; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 14; Journal Issue: 5; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES; Biogeochemistry; Ecosystem ecology; Environmental sciences; Microbial ecology

Citation Formats

Bell, Emma, Lamminmäki, Tiina, Alneberg, Johannes, Andersson, Anders F., Qian, Chen, Xiong, Weili, Hettich, Robert, Frutschi, Manon, and Bernier-Latmani, Rizlan. Active sulfur cycling in the terrestrial deep subsurface. United States: N. p., 2020. Web. doi:10.1038/s41396-020-0602-x.
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Bell, Emma, Lamminmäki, Tiina, Alneberg, Johannes, Andersson, Anders F., Qian, Chen, Xiong, Weili, Hettich, Robert, Frutschi, Manon, & Bernier-Latmani, Rizlan. Active sulfur cycling in the terrestrial deep subsurface. United States. https://doi.org/10.1038/s41396-020-0602-x
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Bell, Emma, Lamminmäki, Tiina, Alneberg, Johannes, Andersson, Anders F., Qian, Chen, Xiong, Weili, Hettich, Robert, Frutschi, Manon, and Bernier-Latmani, Rizlan. Tue . "Active sulfur cycling in the terrestrial deep subsurface". United States. https://doi.org/10.1038/s41396-020-0602-x. https://www.osti.gov/servlets/purl/1606636.
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@article{osti_1606636,
title = {Active sulfur cycling in the terrestrial deep subsurface},
author = {Bell, Emma and Lamminmäki, Tiina and Alneberg, Johannes and Andersson, Anders F. and Qian, Chen and Xiong, Weili and Hettich, Robert and Frutschi, Manon and Bernier-Latmani, Rizlan},
abstractNote = {The deep terrestrial subsurface remains an environment where there is limited understanding of the extant microbial metabolisms. At Olkiluoto, Finland, a deep geological repository is under construction for the final storage of spent nuclear fuel. It is therefore critical to evaluate the potential impact microbial metabolism, including sulfide generation, could have upon the safety of the repository. As such, we investigated a deep groundwater where sulfate is present, but groundwater geochemistry suggests limited microbial sulfate-reducing activity. Examination of the microbial community at the genome-level revealed microorganisms with the metabolic capacity for both oxidative and reductive sulfur transformations. Deltaproteobacteria are shown to have the genetic capacity for sulfate reduction and possibly sulfur disproportionation, while Rhizobiaceae, Rhodocyclaceae, Sideroxydans, and Sulfurimonas oxidize reduced sulfur compounds. Further examination of the proteome confirmed an active sulfur cycle, serving for microbial energy generation and growth. Our results reveal that this sulfide-poor groundwater harbors an active microbial community of sulfate-reducing and sulfide-oxidizing bacteria, together mediating a sulfur cycle that remained undetected by geochemical monitoring alone. The ability of sulfide-oxidizing bacteria to limit the accumulation of sulfide was further demonstrated in groundwater incubations and highlights a potential sink for sulfide that could be beneficial for geological repository safety.},
doi = {10.1038/s41396-020-0602-x},
journal = {The ISME Journal},
number = 5,
volume = 14,
place = {United States},
year = {Tue Feb 11 00:00:00 EST 2020},
month = {Tue Feb 11 00:00:00 EST 2020}
}
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