Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium <italic toggle="yes">Desulfurivibrio alkaliphilus</italic> by Sulfide Oxidation with Nitrate

ABSTRACT This study demonstrates that the deltaproteobacterium Desulfurivibrio alkaliphilus can grow chemolithotrophically by coupling sulfide oxidation to the dissimilatory reduction of nitrate and nitrite to ammonium. Key genes of known sulfide oxidation pathways are absent from the genome of D. a...

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Autores principales: Casper Thorup, Andreas Schramm, Alyssa J. Findlay, Kai W. Finster, Lars Schreiber
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Publicado: American Society for Microbiology 2017
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Acceso en línea:https://doaj.org/article/b3fcc7db8dfc43a6b66058f4a242fe9a
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spelling oai:doaj.org-article:b3fcc7db8dfc43a6b66058f4a242fe9a2021-11-15T15:51:44ZDisguised as a Sulfate Reducer: Growth of the Deltaproteobacterium <italic toggle="yes">Desulfurivibrio alkaliphilus</italic> by Sulfide Oxidation with Nitrate10.1128/mBio.00671-172150-7511https://doaj.org/article/b3fcc7db8dfc43a6b66058f4a242fe9a2017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00671-17https://doaj.org/toc/2150-7511ABSTRACT This study demonstrates that the deltaproteobacterium Desulfurivibrio alkaliphilus can grow chemolithotrophically by coupling sulfide oxidation to the dissimilatory reduction of nitrate and nitrite to ammonium. Key genes of known sulfide oxidation pathways are absent from the genome of D. alkaliphilus. Instead, the genome contains all of the genes necessary for sulfate reduction, including a gene for a reductive-type dissimilatory bisulfite reductase (DSR). Despite this, growth by sulfate reduction was not observed. Transcriptomic analysis revealed a very high expression level of sulfate-reduction genes during growth by sulfide oxidation, while inhibition experiments with molybdate pointed to elemental sulfur/polysulfides as intermediates. Consequently, we propose that D. alkaliphilus initially oxidizes sulfide to elemental sulfur, which is then either disproportionated, or oxidized by a reversal of the sulfate reduction pathway. This is the first study providing evidence that a reductive-type DSR is involved in a sulfide oxidation pathway. Transcriptome sequencing further suggests that nitrate reduction to ammonium is performed by a novel type of periplasmic nitrate reductase and an unusual membrane-anchored nitrite reductase. IMPORTANCE Sulfide oxidation and sulfate reduction, the two major branches of the sulfur cycle, are usually ascribed to distinct sets of microbes with distinct diagnostic genes. Here we show a more complex picture, as D. alkaliphilus, with the genomic setup of a sulfate reducer, grows by sulfide oxidation. The high expression of genes typically involved in the sulfate reduction pathway suggests that these genes, including the reductive-type dissimilatory bisulfite reductases, are also involved in as-yet-unresolved sulfide oxidation pathways. Finally, D. alkaliphilus is closely related to cable bacteria, which grow by electrogenic sulfide oxidation. Since there are no pure cultures of cable bacteria, D. alkaliphilus may represent an exciting model organism in which to study the physiology of this process.Casper ThorupAndreas SchrammAlyssa J. FindlayKai W. FinsterLars SchreiberAmerican Society for MicrobiologyarticleDNRADSRnitrate reductionnitrite reductionsulfate reductionsulfide oxidationMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution DOAJ
collection DOAJ
language EN
topic DNRA
DSR
nitrate reduction
nitrite reduction
sulfate reduction
sulfide oxidation
Microbiology
QR1-502
spellingShingle DNRA
DSR
nitrate reduction
nitrite reduction
sulfate reduction
sulfide oxidation
Microbiology
QR1-502
Casper Thorup
Andreas Schramm
Alyssa J. Findlay
Kai W. Finster
Lars Schreiber
Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium <italic toggle="yes">Desulfurivibrio alkaliphilus</italic> by Sulfide Oxidation with Nitrate
description ABSTRACT This study demonstrates that the deltaproteobacterium Desulfurivibrio alkaliphilus can grow chemolithotrophically by coupling sulfide oxidation to the dissimilatory reduction of nitrate and nitrite to ammonium. Key genes of known sulfide oxidation pathways are absent from the genome of D. alkaliphilus. Instead, the genome contains all of the genes necessary for sulfate reduction, including a gene for a reductive-type dissimilatory bisulfite reductase (DSR). Despite this, growth by sulfate reduction was not observed. Transcriptomic analysis revealed a very high expression level of sulfate-reduction genes during growth by sulfide oxidation, while inhibition experiments with molybdate pointed to elemental sulfur/polysulfides as intermediates. Consequently, we propose that D. alkaliphilus initially oxidizes sulfide to elemental sulfur, which is then either disproportionated, or oxidized by a reversal of the sulfate reduction pathway. This is the first study providing evidence that a reductive-type DSR is involved in a sulfide oxidation pathway. Transcriptome sequencing further suggests that nitrate reduction to ammonium is performed by a novel type of periplasmic nitrate reductase and an unusual membrane-anchored nitrite reductase. IMPORTANCE Sulfide oxidation and sulfate reduction, the two major branches of the sulfur cycle, are usually ascribed to distinct sets of microbes with distinct diagnostic genes. Here we show a more complex picture, as D. alkaliphilus, with the genomic setup of a sulfate reducer, grows by sulfide oxidation. The high expression of genes typically involved in the sulfate reduction pathway suggests that these genes, including the reductive-type dissimilatory bisulfite reductases, are also involved in as-yet-unresolved sulfide oxidation pathways. Finally, D. alkaliphilus is closely related to cable bacteria, which grow by electrogenic sulfide oxidation. Since there are no pure cultures of cable bacteria, D. alkaliphilus may represent an exciting model organism in which to study the physiology of this process.
format article
author Casper Thorup
Andreas Schramm
Alyssa J. Findlay
Kai W. Finster
Lars Schreiber
author_facet Casper Thorup
Andreas Schramm
Alyssa J. Findlay
Kai W. Finster
Lars Schreiber
author_sort Casper Thorup
title Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium <italic toggle="yes">Desulfurivibrio alkaliphilus</italic> by Sulfide Oxidation with Nitrate
title_short Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium <italic toggle="yes">Desulfurivibrio alkaliphilus</italic> by Sulfide Oxidation with Nitrate
title_full Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium <italic toggle="yes">Desulfurivibrio alkaliphilus</italic> by Sulfide Oxidation with Nitrate
title_fullStr Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium <italic toggle="yes">Desulfurivibrio alkaliphilus</italic> by Sulfide Oxidation with Nitrate
title_full_unstemmed Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium <italic toggle="yes">Desulfurivibrio alkaliphilus</italic> by Sulfide Oxidation with Nitrate
title_sort disguised as a sulfate reducer: growth of the deltaproteobacterium <italic toggle="yes">desulfurivibrio alkaliphilus</italic> by sulfide oxidation with nitrate
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/b3fcc7db8dfc43a6b66058f4a242fe9a
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