Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification
Abstract
Competition between nitrate-reducing bacteria (NRB) and sulfate-reducing bacteria (SRB) for resources in anoxic environments is generally thought to be governed largely by thermodynamics. It is now recognized that intermediates of nitrogen and sulfur cycling (e.g., hydrogen sulfide, nitrite, etc.) can also directly impact NRB and SRB activities in freshwater, wastewater, and sediment and therefore may play important roles in competitive interactions. Here, through comparative transcriptomic and metabolomic analyses, we have uncovered mechanisms of hydrogen sulfide- and cysteine-mediated inhibition of nitrate respiratory growth for the NRB Intrasporangium calvum C5. Specifically, the systems analysis predicted that cysteine and hydrogen sulfide inhibit growth of I. calvum C5 by disrupting distinct steps across multiple pathways, including branched-chain amino acid (BCAA) biosynthesis, utilization of specific carbon sources, and cofactor metabolism. We have validated these predictions by demonstrating that complementation with BCAAs and specific carbon sources relieves the growth inhibitory effects of cysteine and hydrogen sulfide. We discuss how these mechanistic insights give new context to the interplay and stratification of NRB and SRB in diverse environments. IMPORTANCE Nitrate-reducing bacteria (NRB) and sulfate-reducing bacteria (SRB) colonize diverse anoxic environments, including soil subsurface, groundwater, and wastewater. NRB and SRB compete for resources, and their interplay has majormore »
- Authors:
-
- Institute for Systems Biology, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States)
- The Scripps Research Inst., La Jolla, CA (United States); State Univ. of New York (SUNY), Syracuse, NY (United States)
- Institute for Systems Biology, Seattle, WA (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- The Scripps Research Inst., La Jolla, CA (United States)
- Univ. of Washington, Seattle, WA (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1767862
- Alternate Identifier(s):
- OSTI ID: 1773755
- Grant/Contract Number:
- AC05-00OR22725; AC02-05CH11231; OCE-1558924; CBET-1606206; MCB-1518261; DBI-1565166; MCB-1616955
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mSystems
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2379-5077
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; cysteine; denitrification; environmental microbiology; hydrogen sulfide; metabolomics; microbial ecology; nitrate-reducing bacteria; systems biology; transcriptomics
Citation Formats
Otwell, Anne E., Carr, Alex V., Majumder, Erica L. W., Ruiz, Maryann K., Wilpiszeski, Regina L., Hoang, Linh T., Webb, Bill, Turkarslan, Serdar, Gibbons, Sean M., Elias, Dwayne A., Stahl, David A., Siuzdak, Gary, and Baliga, Nitin S. Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification. United States: N. p., 2021.
Web. doi:10.1128/msystems.01025-20.
Otwell, Anne E., Carr, Alex V., Majumder, Erica L. W., Ruiz, Maryann K., Wilpiszeski, Regina L., Hoang, Linh T., Webb, Bill, Turkarslan, Serdar, Gibbons, Sean M., Elias, Dwayne A., Stahl, David A., Siuzdak, Gary, & Baliga, Nitin S. Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification. United States. https://doi.org/10.1128/msystems.01025-20
Otwell, Anne E., Carr, Alex V., Majumder, Erica L. W., Ruiz, Maryann K., Wilpiszeski, Regina L., Hoang, Linh T., Webb, Bill, Turkarslan, Serdar, Gibbons, Sean M., Elias, Dwayne A., Stahl, David A., Siuzdak, Gary, and Baliga, Nitin S. Tue .
"Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification". United States. https://doi.org/10.1128/msystems.01025-20. https://www.osti.gov/servlets/purl/1767862.
@article{osti_1767862,
title = {Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification},
author = {Otwell, Anne E. and Carr, Alex V. and Majumder, Erica L. W. and Ruiz, Maryann K. and Wilpiszeski, Regina L. and Hoang, Linh T. and Webb, Bill and Turkarslan, Serdar and Gibbons, Sean M. and Elias, Dwayne A. and Stahl, David A. and Siuzdak, Gary and Baliga, Nitin S.},
abstractNote = {Competition between nitrate-reducing bacteria (NRB) and sulfate-reducing bacteria (SRB) for resources in anoxic environments is generally thought to be governed largely by thermodynamics. It is now recognized that intermediates of nitrogen and sulfur cycling (e.g., hydrogen sulfide, nitrite, etc.) can also directly impact NRB and SRB activities in freshwater, wastewater, and sediment and therefore may play important roles in competitive interactions. Here, through comparative transcriptomic and metabolomic analyses, we have uncovered mechanisms of hydrogen sulfide- and cysteine-mediated inhibition of nitrate respiratory growth for the NRB Intrasporangium calvum C5. Specifically, the systems analysis predicted that cysteine and hydrogen sulfide inhibit growth of I. calvum C5 by disrupting distinct steps across multiple pathways, including branched-chain amino acid (BCAA) biosynthesis, utilization of specific carbon sources, and cofactor metabolism. We have validated these predictions by demonstrating that complementation with BCAAs and specific carbon sources relieves the growth inhibitory effects of cysteine and hydrogen sulfide. We discuss how these mechanistic insights give new context to the interplay and stratification of NRB and SRB in diverse environments. IMPORTANCE Nitrate-reducing bacteria (NRB) and sulfate-reducing bacteria (SRB) colonize diverse anoxic environments, including soil subsurface, groundwater, and wastewater. NRB and SRB compete for resources, and their interplay has major implications on the global cycling of nitrogen and sulfur species, with undesirable outcomes in some contexts. For instance, the removal of reactive nitrogen species by NRB is desirable for wastewater treatment, but in agricultural soils, NRB can drive the conversion of nitrates from fertilizers into nitrous oxide, a potent greenhouse gas. Similarly, the hydrogen sulfide produced by SRB can help sequester and immobilize toxic heavy metals but is undesirable in oil wells where competition between SRB and NRB has been exploited to suppress hydrogen sulfide production. By characterizing how reduced sulfur compounds inhibit growth and activity of NRB, we have gained systems-level and mechanistic insight into the interplay of these two important groups of organisms and drivers of their stratification in diverse environments.},
doi = {10.1128/msystems.01025-20},
journal = {mSystems},
number = 1,
volume = 6,
place = {United States},
year = {Tue Feb 09 00:00:00 EST 2021},
month = {Tue Feb 09 00:00:00 EST 2021}
}
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