Mechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS

ABSTRACT The genetic and biochemical basis of perchlorate-dependent H2S oxidation (PSOX) was investigated in the dissimilatory perchlorate-reducing microorganism (DPRM) Azospira suillum PS (PS). Previously, it was shown that all known DPRMs innately oxidize H2S, producing elemental sulfur (So). Alth...

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Autores principales:	Misha G. Mehta-Kolte, Dana Loutey, Ouwei Wang, Matthew D. Youngblut, Christopher G. Hubbard, Kelly M. Wetmore, Mark E. Conrad, John D. Coates
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5f3cf7c7ee3c4096bdbe43566c1f5071
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spelling	oai:doaj.org-article:5f3cf7c7ee3c4096bdbe43566c1f50712021-11-15T15:51:07ZMechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS10.1128/mBio.02023-162150-7511https://doaj.org/article/5f3cf7c7ee3c4096bdbe43566c1f50712017-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02023-16https://doaj.org/toc/2150-7511ABSTRACT The genetic and biochemical basis of perchlorate-dependent H2S oxidation (PSOX) was investigated in the dissimilatory perchlorate-reducing microorganism (DPRM) Azospira suillum PS (PS). Previously, it was shown that all known DPRMs innately oxidize H2S, producing elemental sulfur (So). Although the process involving PSOX is thermodynamically favorable (ΔG°′ = −206 kJ ⋅ mol−1 H2S), the underlying biochemical and genetic mechanisms are currently unknown. Interestingly, H2S is preferentially utilized over physiological electron donors such as lactate or acetate although no growth benefit is obtained from the metabolism. Here, we determined that PSOX is due to a combination of enzymatic and abiotic interactions involving reactive intermediates of perchlorate respiration. Using various approaches, including barcode analysis by sequencing (Bar-seq), transcriptome sequencing (RNA-seq), and proteomics, along with targeted mutagenesis and biochemical characterization, we identified all facets of PSOX in PS. In support of our proposed model, deletion of identified upregulated PS genes traditionally known to be involved in sulfur redox cycling (e.g., Sox, sulfide:quinone reductase [SQR]) showed no defect in PSOX activity. Proteomic analysis revealed differential abundances of a variety of stress response metal efflux pumps and divalent heavy-metal transporter proteins, suggesting a general toxicity response. Furthermore, in vitro biochemical studies demonstrated direct PSOX mediated by purified perchlorate reductase (PcrAB) in the absence of other electron transfer proteins. The results of these studies support a model in which H2S oxidation is mediated by electron transport chain short-circuiting in the periplasmic space where the PcrAB directly oxidizes H2S to So. The biogenically formed reactive intermediates (ClO2− and O2) subsequently react with additional H2S, producing polysulfide and So as end products. IMPORTANCE Inorganic sulfur compounds are widespread in nature, and microorganisms are central to their transformation, thereby playing a key role in the global sulfur cycle. Sulfur oxidation is mediated by a broad phylogenetic diversity of microorganisms, including anoxygenic phototrophs and either aerobic or anaerobic chemotrophs coupled to oxygen or nitrate respiration, respectively. Recently, perchlorate-respiring microorganisms were demonstrated to be innately capable of sulfur oxidation regardless of their phylogenetic affiliation. As recognition of the prevalence of these organisms intensifies, their role in global geochemical cycles is being queried. This is further highlighted by the recently recognized environmental pervasiveness of perchlorate not only across Earth but also throughout our solar system. The inferred importance of this metabolism not only is that it is a novel and previously unrecognized component of the global sulfur redox cycle but also is because of the recently demonstrated applicability of perchlorate respiration in the control of biogenic sulfide production in engineered environments such as oil reservoirs and wastewater treatment facilities, where excess H2S represents a significant environmental, process, and health risk, with associated costs approximating $90 billion annually.Misha G. Mehta-KolteDana LouteyOuwei WangMatthew D. YoungblutChristopher G. HubbardKelly M. WetmoreMark E. ConradJohn D. CoatesAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 8, Iss 1 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Misha G. Mehta-Kolte Dana Loutey Ouwei Wang Matthew D. Youngblut Christopher G. Hubbard Kelly M. Wetmore Mark E. Conrad John D. Coates Mechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS
description	ABSTRACT The genetic and biochemical basis of perchlorate-dependent H2S oxidation (PSOX) was investigated in the dissimilatory perchlorate-reducing microorganism (DPRM) Azospira suillum PS (PS). Previously, it was shown that all known DPRMs innately oxidize H2S, producing elemental sulfur (So). Although the process involving PSOX is thermodynamically favorable (ΔG°′ = −206 kJ ⋅ mol−1 H2S), the underlying biochemical and genetic mechanisms are currently unknown. Interestingly, H2S is preferentially utilized over physiological electron donors such as lactate or acetate although no growth benefit is obtained from the metabolism. Here, we determined that PSOX is due to a combination of enzymatic and abiotic interactions involving reactive intermediates of perchlorate respiration. Using various approaches, including barcode analysis by sequencing (Bar-seq), transcriptome sequencing (RNA-seq), and proteomics, along with targeted mutagenesis and biochemical characterization, we identified all facets of PSOX in PS. In support of our proposed model, deletion of identified upregulated PS genes traditionally known to be involved in sulfur redox cycling (e.g., Sox, sulfide:quinone reductase [SQR]) showed no defect in PSOX activity. Proteomic analysis revealed differential abundances of a variety of stress response metal efflux pumps and divalent heavy-metal transporter proteins, suggesting a general toxicity response. Furthermore, in vitro biochemical studies demonstrated direct PSOX mediated by purified perchlorate reductase (PcrAB) in the absence of other electron transfer proteins. The results of these studies support a model in which H2S oxidation is mediated by electron transport chain short-circuiting in the periplasmic space where the PcrAB directly oxidizes H2S to So. The biogenically formed reactive intermediates (ClO2− and O2) subsequently react with additional H2S, producing polysulfide and So as end products. IMPORTANCE Inorganic sulfur compounds are widespread in nature, and microorganisms are central to their transformation, thereby playing a key role in the global sulfur cycle. Sulfur oxidation is mediated by a broad phylogenetic diversity of microorganisms, including anoxygenic phototrophs and either aerobic or anaerobic chemotrophs coupled to oxygen or nitrate respiration, respectively. Recently, perchlorate-respiring microorganisms were demonstrated to be innately capable of sulfur oxidation regardless of their phylogenetic affiliation. As recognition of the prevalence of these organisms intensifies, their role in global geochemical cycles is being queried. This is further highlighted by the recently recognized environmental pervasiveness of perchlorate not only across Earth but also throughout our solar system. The inferred importance of this metabolism not only is that it is a novel and previously unrecognized component of the global sulfur redox cycle but also is because of the recently demonstrated applicability of perchlorate respiration in the control of biogenic sulfide production in engineered environments such as oil reservoirs and wastewater treatment facilities, where excess H2S represents a significant environmental, process, and health risk, with associated costs approximating $90 billion annually.
format	article
author	Misha G. Mehta-Kolte Dana Loutey Ouwei Wang Matthew D. Youngblut Christopher G. Hubbard Kelly M. Wetmore Mark E. Conrad John D. Coates
author_facet	Misha G. Mehta-Kolte Dana Loutey Ouwei Wang Matthew D. Youngblut Christopher G. Hubbard Kelly M. Wetmore Mark E. Conrad John D. Coates
author_sort	Misha G. Mehta-Kolte
title	Mechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS
title_short	Mechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS
title_full	Mechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS
title_fullStr	Mechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS
title_full_unstemmed	Mechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS
title_sort	mechanism of h<sub>2</sub>s oxidation by the dissimilatory perchlorate-reducing microorganism <italic toggle="yes">azospira suillum</italic> ps
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/5f3cf7c7ee3c4096bdbe43566c1f5071
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Mechanism of H<sub>2</sub>S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism <italic toggle="yes">Azospira suillum</italic> PS

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