Mechanism of H2S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism Azospira suillum 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). 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 bymore »
- Authors:
-
- Univ. of California, Berkeley, CA (United States). Energy Biosciences Inst.
- Univ. of California, Berkeley, CA (United States). Energy Biosciences Inst.; Univ. of California, Berkeley, CA (United States). Plant and Microbial Biology Dept.
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences Area
- Univ. of California, Berkeley, CA (United States). Energy Biosciences Inst.; Univ. of California, Berkeley, CA (United States). Plant and Microbial Biology Dept.
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1626142
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology (ASM)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; microbiology
Citation Formats
Mehta-Kolte, Misha G., Loutey, Dana, Wang, Ouwei, Youngblut, Matthew D., Hubbard, Christopher G., Wetmore, Kelly M., Conrad, Mark E., and Coates, John D. Mechanism of H2S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism Azospira suillum PS. United States: N. p., 2017.
Web. doi:10.1128/mbio.02023-16.
Mehta-Kolte, Misha G., Loutey, Dana, Wang, Ouwei, Youngblut, Matthew D., Hubbard, Christopher G., Wetmore, Kelly M., Conrad, Mark E., & Coates, John D. Mechanism of H2S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism Azospira suillum PS. United States. https://doi.org/10.1128/mbio.02023-16
Mehta-Kolte, Misha G., Loutey, Dana, Wang, Ouwei, Youngblut, Matthew D., Hubbard, Christopher G., Wetmore, Kelly M., Conrad, Mark E., and Coates, John D. Tue .
"Mechanism of H2S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism Azospira suillum PS". United States. https://doi.org/10.1128/mbio.02023-16. https://www.osti.gov/servlets/purl/1626142.
@article{osti_1626142,
title = {Mechanism of H2S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism Azospira suillum PS},
author = {Mehta-Kolte, Misha G. and Loutey, Dana and Wang, Ouwei and Youngblut, Matthew D. and Hubbard, Christopher G. and Wetmore, Kelly M. and Conrad, Mark E. and Coates, John D.},
abstractNote = {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.},
doi = {10.1128/mbio.02023-16},
journal = {mBio (Online)},
number = 1,
volume = 8,
place = {United States},
year = {Tue Feb 21 00:00:00 EST 2017},
month = {Tue Feb 21 00:00:00 EST 2017}
}
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Works referencing / citing this record:
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