Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>

ABSTRACT Rhodospirillum rubrum possesses a novel oxygen-independent, aerobic methionine salvage pathway (MSP) for recycling methionine from 5-methylthioadenosine (MTA), the MTA-isoprenoid shunt. This organism can also metabolize MTA as a sulfur source under anaerobic conditions, suggesting that the...

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Autores principales:	Justin A. North, Jaya Sriram, Karuna Chourey, Christopher D. Ecker, Ritin Sharma, John A. Wildenthal, Robert L. Hettich, F. Robert Tabita
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Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5809a96fff0f4ac8a287d88dbe90726e
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spelling	oai:doaj.org-article:5809a96fff0f4ac8a287d88dbe90726e2021-11-15T15:50:18ZMetabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>10.1128/mBio.00855-162150-7511https://doaj.org/article/5809a96fff0f4ac8a287d88dbe90726e2016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00855-16https://doaj.org/toc/2150-7511ABSTRACT Rhodospirillum rubrum possesses a novel oxygen-independent, aerobic methionine salvage pathway (MSP) for recycling methionine from 5-methylthioadenosine (MTA), the MTA-isoprenoid shunt. This organism can also metabolize MTA as a sulfur source under anaerobic conditions, suggesting that the MTA-isoprenoid shunt may also function anaerobically as well. In this study, deep proteomics profiling, directed metabolite analysis, and reverse transcriptase quantitative PCR (RT-qPCR) revealed metabolic changes in response to anaerobic growth on MTA versus sulfate as sole sulfur source. The abundance of protein levels associated with methionine transport, cell motility, and chemotaxis increased in the presence of MTA over that in the presence of sulfate. Purine salvage from MTA resulted primarily in hypoxanthine accumulation and a decrease in protein levels involved in GMP-to-AMP conversion to balance purine pools. Acyl coenzyme A (acyl-CoA) metabolic protein levels for lipid metabolism were lower in abundance, whereas poly-β-hydroxybutyrate synthesis and storage were increased nearly 10-fold. The known R. rubrum aerobic MSP was also shown to be upregulated, to function anaerobically, and to recycle MTA. This suggested that other organisms with gene homologues for the MTA-isoprenoid shunt may also possess a functioning anaerobic MSP. In support of our previous findings that ribulose-1,5-carboxylase/oxygenase (RubisCO) is required for an apparently purely anaerobic MSP, RubisCO transcript and protein levels both increased in abundance by over 10-fold in cells grown anaerobically on MTA over those in cells grown on sulfate, resulting in increased intracellular RubisCO activity. These results reveal for the first time global metabolic responses as a consequence of anaerobic MTA metabolism compared to using sulfate as the sulfur source. IMPORTANCE In nearly all organisms, sulfur-containing byproducts result from many metabolic reactions. Unless these compounds are further metabolized, valuable organic sulfur is lost and can become limiting. To regenerate the sulfur-containing amino acid methionine, organisms typically employ one of several variations of a “universal” methionine salvage pathway (MSP). A common aspect of the universal MSP is a final oxygenation step. This work establishes that the metabolically versatile bacterium Rhodospirillum rubrum employs a novel MSP that does not require oxygen under either aerobic or anaerobic conditions. There is also a separate, dedicated anaerobic MTA metabolic route in R. rubrum. This work reveals global changes in cellular metabolism in response to anaerobic MTA metabolism compared to using sulfate as a sulfur source. We found that cell mobility and transport were enhanced, along with lipid, nucleotide, and carbohydrate metabolism, when cells were grown in the presence of MTA.Justin A. NorthJaya SriramKaruna ChoureyChristopher D. EckerRitin SharmaJohn A. WildenthalRobert L. HettichF. Robert TabitaAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Justin A. North Jaya Sriram Karuna Chourey Christopher D. Ecker Ritin Sharma John A. Wildenthal Robert L. Hettich F. Robert Tabita Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>
description	ABSTRACT Rhodospirillum rubrum possesses a novel oxygen-independent, aerobic methionine salvage pathway (MSP) for recycling methionine from 5-methylthioadenosine (MTA), the MTA-isoprenoid shunt. This organism can also metabolize MTA as a sulfur source under anaerobic conditions, suggesting that the MTA-isoprenoid shunt may also function anaerobically as well. In this study, deep proteomics profiling, directed metabolite analysis, and reverse transcriptase quantitative PCR (RT-qPCR) revealed metabolic changes in response to anaerobic growth on MTA versus sulfate as sole sulfur source. The abundance of protein levels associated with methionine transport, cell motility, and chemotaxis increased in the presence of MTA over that in the presence of sulfate. Purine salvage from MTA resulted primarily in hypoxanthine accumulation and a decrease in protein levels involved in GMP-to-AMP conversion to balance purine pools. Acyl coenzyme A (acyl-CoA) metabolic protein levels for lipid metabolism were lower in abundance, whereas poly-β-hydroxybutyrate synthesis and storage were increased nearly 10-fold. The known R. rubrum aerobic MSP was also shown to be upregulated, to function anaerobically, and to recycle MTA. This suggested that other organisms with gene homologues for the MTA-isoprenoid shunt may also possess a functioning anaerobic MSP. In support of our previous findings that ribulose-1,5-carboxylase/oxygenase (RubisCO) is required for an apparently purely anaerobic MSP, RubisCO transcript and protein levels both increased in abundance by over 10-fold in cells grown anaerobically on MTA over those in cells grown on sulfate, resulting in increased intracellular RubisCO activity. These results reveal for the first time global metabolic responses as a consequence of anaerobic MTA metabolism compared to using sulfate as the sulfur source. IMPORTANCE In nearly all organisms, sulfur-containing byproducts result from many metabolic reactions. Unless these compounds are further metabolized, valuable organic sulfur is lost and can become limiting. To regenerate the sulfur-containing amino acid methionine, organisms typically employ one of several variations of a “universal” methionine salvage pathway (MSP). A common aspect of the universal MSP is a final oxygenation step. This work establishes that the metabolically versatile bacterium Rhodospirillum rubrum employs a novel MSP that does not require oxygen under either aerobic or anaerobic conditions. There is also a separate, dedicated anaerobic MTA metabolic route in R. rubrum. This work reveals global changes in cellular metabolism in response to anaerobic MTA metabolism compared to using sulfate as a sulfur source. We found that cell mobility and transport were enhanced, along with lipid, nucleotide, and carbohydrate metabolism, when cells were grown in the presence of MTA.
format	article
author	Justin A. North Jaya Sriram Karuna Chourey Christopher D. Ecker Ritin Sharma John A. Wildenthal Robert L. Hettich F. Robert Tabita
author_facet	Justin A. North Jaya Sriram Karuna Chourey Christopher D. Ecker Ritin Sharma John A. Wildenthal Robert L. Hettich F. Robert Tabita
author_sort	Justin A. North
title	Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>
title_short	Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>
title_full	Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>
title_fullStr	Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>
title_full_unstemmed	Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>
title_sort	metabolic regulation as a consequence of anaerobic 5-methylthioadenosine recycling in <named-content content-type="genus-species">rhodospirillum rubrum</named-content>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/5809a96fff0f4ac8a287d88dbe90726e
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Metabolic Regulation as a Consequence of Anaerobic 5-Methylthioadenosine Recycling in <named-content content-type="genus-species">Rhodospirillum rubrum</named-content>

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