Two Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>

ABSTRACT 5′-Methyl-thioadenosine (MTA) is a dead-end, sulfur-containing metabolite and cellular inhibitor that arises from S-adenosyl-l-methionine-dependent reactions. Recent studies have indicated that there are diverse bacterial methionine salvage pathways (MSPs) for MTA detoxification and sulfur...

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Autores principales:	Anthony R. Miller, Justin A. North, John A. Wildenthal, F. Robert Tabita
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Rhodopseudomonas palustris methanethiol methionine salvage Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7ea55d56e97346fda314287398f228cb
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spelling	oai:doaj.org-article:7ea55d56e97346fda314287398f228cb2021-11-15T15:53:26ZTwo Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>10.1128/mBio.00407-182150-7511https://doaj.org/article/7ea55d56e97346fda314287398f228cb2018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00407-18https://doaj.org/toc/2150-7511ABSTRACT 5′-Methyl-thioadenosine (MTA) is a dead-end, sulfur-containing metabolite and cellular inhibitor that arises from S-adenosyl-l-methionine-dependent reactions. Recent studies have indicated that there are diverse bacterial methionine salvage pathways (MSPs) for MTA detoxification and sulfur salvage. Here, via a combination of gene deletions and directed metabolite detection studies, we report that under aerobic conditions the facultatively anaerobic bacterium Rhodopseudomonas palustris employs both an MTA-isoprenoid shunt identical to that previously described in Rhodospirillum rubrum and a second novel MSP, both of which generate a methanethiol intermediate. The additional R. palustris aerobic MSP, a dihydroxyacetone phosphate (DHAP)-methanethiol shunt, initially converts MTA to 2-(methylthio)ethanol and DHAP. This is identical to the initial steps of the recently reported anaerobic ethylene-forming MSP, the DHAP-ethylene shunt. The aerobic DHAP-methanethiol shunt then further metabolizes 2-(methylthio)ethanol to methanethiol, which can be directly utilized by O-acetyl-l-homoserine sulfhydrylase to regenerate methionine. This is in contrast to the anaerobic DHAP-ethylene shunt, which metabolizes 2-(methylthio)ethanol to ethylene and an unknown organo-sulfur intermediate, revealing functional diversity in MSPs utilizing a 2-(methylthio)ethanol intermediate. When MTA was fed to aerobically growing cells, the rate of volatile methanethiol release was constant irrespective of the presence of sulfate, suggesting a general housekeeping function for these MSPs up through the methanethiol production step. Methanethiol and dimethyl sulfide (DMS), two of the most important compounds of the global sulfur cycle, appear to arise not only from marine ecosystems but from terrestrial ones as well. These results reveal a possible route by which methanethiol might be biologically produced in soil and freshwater environments. IMPORTANCE Biologically available sulfur is often limiting in the environment. Therefore, many organisms have developed methionine salvage pathways (MSPs) to recycle sulfur-containing by-products back into the amino acid methionine. The metabolically versatile bacterium Rhodopseudomonas palustris is unusual in that it possesses two RuBisCOs and two RuBisCO-like proteins. While RuBisCO primarily serves as the carbon fixation enzyme of the Calvin cycle, RuBisCOs and certain RuBisCO-like proteins have also been shown to function in methionine salvage. This work establishes that only one of the R. palustris RuBisCO-like proteins functions as part of an MSP. Moreover, in the presence of oxygen, to salvage sulfur, R. palustris employs two pathways, both of which result in production of volatile methanethiol, a key compound of the global sulfur cycle. When total available sulfur was plentiful, methanethiol was readily released into the environment. However, when sulfur became limiting, methanethiol release decreased, presumably due to methanethiol utilization to regenerate needed methionine.Anthony R. MillerJustin A. NorthJohn A. WildenthalF. Robert TabitaAmerican Society for MicrobiologyarticleRhodopseudomonas palustrismethanethiolmethionine salvageMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Rhodopseudomonas palustris methanethiol methionine salvage Microbiology QR1-502
spellingShingle	Rhodopseudomonas palustris methanethiol methionine salvage Microbiology QR1-502 Anthony R. Miller Justin A. North John A. Wildenthal F. Robert Tabita Two Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>
description	ABSTRACT 5′-Methyl-thioadenosine (MTA) is a dead-end, sulfur-containing metabolite and cellular inhibitor that arises from S-adenosyl-l-methionine-dependent reactions. Recent studies have indicated that there are diverse bacterial methionine salvage pathways (MSPs) for MTA detoxification and sulfur salvage. Here, via a combination of gene deletions and directed metabolite detection studies, we report that under aerobic conditions the facultatively anaerobic bacterium Rhodopseudomonas palustris employs both an MTA-isoprenoid shunt identical to that previously described in Rhodospirillum rubrum and a second novel MSP, both of which generate a methanethiol intermediate. The additional R. palustris aerobic MSP, a dihydroxyacetone phosphate (DHAP)-methanethiol shunt, initially converts MTA to 2-(methylthio)ethanol and DHAP. This is identical to the initial steps of the recently reported anaerobic ethylene-forming MSP, the DHAP-ethylene shunt. The aerobic DHAP-methanethiol shunt then further metabolizes 2-(methylthio)ethanol to methanethiol, which can be directly utilized by O-acetyl-l-homoserine sulfhydrylase to regenerate methionine. This is in contrast to the anaerobic DHAP-ethylene shunt, which metabolizes 2-(methylthio)ethanol to ethylene and an unknown organo-sulfur intermediate, revealing functional diversity in MSPs utilizing a 2-(methylthio)ethanol intermediate. When MTA was fed to aerobically growing cells, the rate of volatile methanethiol release was constant irrespective of the presence of sulfate, suggesting a general housekeeping function for these MSPs up through the methanethiol production step. Methanethiol and dimethyl sulfide (DMS), two of the most important compounds of the global sulfur cycle, appear to arise not only from marine ecosystems but from terrestrial ones as well. These results reveal a possible route by which methanethiol might be biologically produced in soil and freshwater environments. IMPORTANCE Biologically available sulfur is often limiting in the environment. Therefore, many organisms have developed methionine salvage pathways (MSPs) to recycle sulfur-containing by-products back into the amino acid methionine. The metabolically versatile bacterium Rhodopseudomonas palustris is unusual in that it possesses two RuBisCOs and two RuBisCO-like proteins. While RuBisCO primarily serves as the carbon fixation enzyme of the Calvin cycle, RuBisCOs and certain RuBisCO-like proteins have also been shown to function in methionine salvage. This work establishes that only one of the R. palustris RuBisCO-like proteins functions as part of an MSP. Moreover, in the presence of oxygen, to salvage sulfur, R. palustris employs two pathways, both of which result in production of volatile methanethiol, a key compound of the global sulfur cycle. When total available sulfur was plentiful, methanethiol was readily released into the environment. However, when sulfur became limiting, methanethiol release decreased, presumably due to methanethiol utilization to regenerate needed methionine.
format	article
author	Anthony R. Miller Justin A. North John A. Wildenthal F. Robert Tabita
author_facet	Anthony R. Miller Justin A. North John A. Wildenthal F. Robert Tabita
author_sort	Anthony R. Miller
title	Two Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>
title_short	Two Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>
title_full	Two Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>
title_fullStr	Two Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>
title_full_unstemmed	Two Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>
title_sort	two distinct aerobic methionine salvage pathways generate volatile methanethiol in <named-content content-type="genus-species">rhodopseudomonas palustris</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/7ea55d56e97346fda314287398f228cb
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Two Distinct Aerobic Methionine Salvage Pathways Generate Volatile Methanethiol in <named-content content-type="genus-species">Rhodopseudomonas palustris</named-content>

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