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...

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Autores principales:	Anne E. Otwell, Alex V. Carr, Erica L. W. Majumder, Maryann K. Ruiz, Regina L. Wilpiszeski, Linh T. Hoang, Bill Webb, Serdar Turkarslan, Sean M. Gibbons, Dwayne A. Elias, David A. Stahl, Gary Siuzdak, Nitin S. Baliga
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	cysteine denitrification environmental microbiology hydrogen sulfide metabolomics microbial ecology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ba6e671d182047fbaa3417e72f526017
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spelling	oai:doaj.org-article:ba6e671d182047fbaa3417e72f5260172021-12-02T18:20:19ZSulfur Metabolites Play Key System-Level Roles in Modulating Denitrification10.1128/mSystems.01025-202379-5077https://doaj.org/article/ba6e671d182047fbaa3417e72f5260172021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01025-20https://doaj.org/toc/2379-5077ABSTRACT 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.Anne E. OtwellAlex V. CarrErica L. W. MajumderMaryann K. RuizRegina L. WilpiszeskiLinh T. HoangBill WebbSerdar TurkarslanSean M. GibbonsDwayne A. EliasDavid A. StahlGary SiuzdakNitin S. BaligaAmerican Society for Microbiologyarticlecysteinedenitrificationenvironmental microbiologyhydrogen sulfidemetabolomicsmicrobial ecologyMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	cysteine denitrification environmental microbiology hydrogen sulfide metabolomics microbial ecology Microbiology QR1-502
spellingShingle	cysteine denitrification environmental microbiology hydrogen sulfide metabolomics microbial ecology Microbiology QR1-502 Anne E. Otwell Alex V. Carr Erica L. W. Majumder Maryann K. Ruiz Regina L. Wilpiszeski Linh T. Hoang Bill Webb Serdar Turkarslan Sean M. Gibbons Dwayne A. Elias David A. Stahl Gary Siuzdak Nitin S. Baliga Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification
description	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 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.
format	article
author	Anne E. Otwell Alex V. Carr Erica L. W. Majumder Maryann K. Ruiz Regina L. Wilpiszeski Linh T. Hoang Bill Webb Serdar Turkarslan Sean M. Gibbons Dwayne A. Elias David A. Stahl Gary Siuzdak Nitin S. Baliga
author_facet	Anne E. Otwell Alex V. Carr Erica L. W. Majumder Maryann K. Ruiz Regina L. Wilpiszeski Linh T. Hoang Bill Webb Serdar Turkarslan Sean M. Gibbons Dwayne A. Elias David A. Stahl Gary Siuzdak Nitin S. Baliga
author_sort	Anne E. Otwell
title	Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification
title_short	Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification
title_full	Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification
title_fullStr	Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification
title_full_unstemmed	Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification
title_sort	sulfur metabolites play key system-level roles in modulating denitrification
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/ba6e671d182047fbaa3417e72f526017
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Sulfur Metabolites Play Key System-Level Roles in Modulating Denitrification

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