Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation

ABSTRACT Syntrophus aciditrophicus is a model syntrophic bacterium that degrades key intermediates in anaerobic decomposition, such as benzoate, cyclohexane-1-carboxylate, and certain fatty acids, to acetate when grown with hydrogen-/formate-consuming microorganisms. ATP formation coupled to acetate...

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Autores principales:	Kimberly L. James, Luis A. Ríos-Hernández, Neil Q. Wofford, Housna Mouttaki, Jessica R. Sieber, Cody S. Sheik, Hong H. Nguyen, Yanan Yang, Yongming Xie, Jonathan Erde, Lars Rohlin, Elizabeth A. Karr, Joseph A. Loo, Rachel R. Ogorzalek Loo, Gregory B. Hurst, Robert P. Gunsalus, Luke I. Szweda, Michael J. McInerney
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d1dab5dbda50462a851bf92528d0875e
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spelling	oai:doaj.org-article:d1dab5dbda50462a851bf92528d0875e2021-11-15T15:50:18ZPyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation10.1128/mBio.01208-162150-7511https://doaj.org/article/d1dab5dbda50462a851bf92528d0875e2016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01208-16https://doaj.org/toc/2150-7511ABSTRACT Syntrophus aciditrophicus is a model syntrophic bacterium that degrades key intermediates in anaerobic decomposition, such as benzoate, cyclohexane-1-carboxylate, and certain fatty acids, to acetate when grown with hydrogen-/formate-consuming microorganisms. ATP formation coupled to acetate production is the main source for energy conservation by S. aciditrophicus. However, the absence of homologs for phosphate acetyltransferase and acetate kinase in the genome of S. aciditrophicus leaves it unclear as to how ATP is formed, as most fermentative bacteria rely on these two enzymes to synthesize ATP from acetyl coenzyme A (CoA) and phosphate. Here, we combine transcriptomic, proteomic, metabolite, and enzymatic approaches to show that S. aciditrophicus uses AMP-forming, acetyl-CoA synthetase (Acs1) for ATP synthesis from acetyl-CoA. acs1 mRNA and Acs1 were abundant in transcriptomes and proteomes, respectively, of S. aciditrophicus grown in pure culture and coculture. Cell extracts of S. aciditrophicus had low or undetectable acetate kinase and phosphate acetyltransferase activities but had high acetyl-CoA synthetase activity under all growth conditions tested. Both Acs1 purified from S. aciditrophicus and recombinantly produced Acs1 catalyzed ATP and acetate formation from acetyl-CoA, AMP, and pyrophosphate. High pyrophosphate levels and a high AMP-to-ATP ratio (5.9 ± 1.4) in S. aciditrophicus cells support the operation of Acs1 in the acetate-forming direction. Thus, S. aciditrophicus has a unique approach to conserve energy involving pyrophosphate, AMP, acetyl-CoA, and an AMP-forming, acetyl-CoA synthetase. IMPORTANCE Bacteria use two enzymes, phosphate acetyltransferase and acetate kinase, to make ATP from acetyl-CoA, while acetate-forming archaea use a single enzyme, an ADP-forming, acetyl-CoA synthetase, to synthesize ATP and acetate from acetyl-CoA. Syntrophus aciditrophicus apparently relies on a different approach to conserve energy during acetyl-CoA metabolism, as its genome does not have homologs to the genes for phosphate acetyltransferase and acetate kinase. Here, we show that S. aciditrophicus uses an alternative approach, an AMP-forming, acetyl-CoA synthetase, to make ATP from acetyl-CoA. AMP-forming, acetyl-CoA synthetases were previously thought to function only in the activation of acetate to acetyl-CoA.Kimberly L. JamesLuis A. Ríos-HernándezNeil Q. WoffordHousna MouttakiJessica R. SieberCody S. SheikHong H. NguyenYanan YangYongming XieJonathan ErdeLars RohlinElizabeth A. KarrJoseph A. LooRachel R. Ogorzalek LooGregory B. HurstRobert P. GunsalusLuke I. SzwedaMichael J. McInerneyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Kimberly L. James Luis A. Ríos-Hernández Neil Q. Wofford Housna Mouttaki Jessica R. Sieber Cody S. Sheik Hong H. Nguyen Yanan Yang Yongming Xie Jonathan Erde Lars Rohlin Elizabeth A. Karr Joseph A. Loo Rachel R. Ogorzalek Loo Gregory B. Hurst Robert P. Gunsalus Luke I. Szweda Michael J. McInerney Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation
description	ABSTRACT Syntrophus aciditrophicus is a model syntrophic bacterium that degrades key intermediates in anaerobic decomposition, such as benzoate, cyclohexane-1-carboxylate, and certain fatty acids, to acetate when grown with hydrogen-/formate-consuming microorganisms. ATP formation coupled to acetate production is the main source for energy conservation by S. aciditrophicus. However, the absence of homologs for phosphate acetyltransferase and acetate kinase in the genome of S. aciditrophicus leaves it unclear as to how ATP is formed, as most fermentative bacteria rely on these two enzymes to synthesize ATP from acetyl coenzyme A (CoA) and phosphate. Here, we combine transcriptomic, proteomic, metabolite, and enzymatic approaches to show that S. aciditrophicus uses AMP-forming, acetyl-CoA synthetase (Acs1) for ATP synthesis from acetyl-CoA. acs1 mRNA and Acs1 were abundant in transcriptomes and proteomes, respectively, of S. aciditrophicus grown in pure culture and coculture. Cell extracts of S. aciditrophicus had low or undetectable acetate kinase and phosphate acetyltransferase activities but had high acetyl-CoA synthetase activity under all growth conditions tested. Both Acs1 purified from S. aciditrophicus and recombinantly produced Acs1 catalyzed ATP and acetate formation from acetyl-CoA, AMP, and pyrophosphate. High pyrophosphate levels and a high AMP-to-ATP ratio (5.9 ± 1.4) in S. aciditrophicus cells support the operation of Acs1 in the acetate-forming direction. Thus, S. aciditrophicus has a unique approach to conserve energy involving pyrophosphate, AMP, acetyl-CoA, and an AMP-forming, acetyl-CoA synthetase. IMPORTANCE Bacteria use two enzymes, phosphate acetyltransferase and acetate kinase, to make ATP from acetyl-CoA, while acetate-forming archaea use a single enzyme, an ADP-forming, acetyl-CoA synthetase, to synthesize ATP and acetate from acetyl-CoA. Syntrophus aciditrophicus apparently relies on a different approach to conserve energy during acetyl-CoA metabolism, as its genome does not have homologs to the genes for phosphate acetyltransferase and acetate kinase. Here, we show that S. aciditrophicus uses an alternative approach, an AMP-forming, acetyl-CoA synthetase, to make ATP from acetyl-CoA. AMP-forming, acetyl-CoA synthetases were previously thought to function only in the activation of acetate to acetyl-CoA.
format	article
author	Kimberly L. James Luis A. Ríos-Hernández Neil Q. Wofford Housna Mouttaki Jessica R. Sieber Cody S. Sheik Hong H. Nguyen Yanan Yang Yongming Xie Jonathan Erde Lars Rohlin Elizabeth A. Karr Joseph A. Loo Rachel R. Ogorzalek Loo Gregory B. Hurst Robert P. Gunsalus Luke I. Szweda Michael J. McInerney
author_facet	Kimberly L. James Luis A. Ríos-Hernández Neil Q. Wofford Housna Mouttaki Jessica R. Sieber Cody S. Sheik Hong H. Nguyen Yanan Yang Yongming Xie Jonathan Erde Lars Rohlin Elizabeth A. Karr Joseph A. Loo Rachel R. Ogorzalek Loo Gregory B. Hurst Robert P. Gunsalus Luke I. Szweda Michael J. McInerney
author_sort	Kimberly L. James
title	Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation
title_short	Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation
title_full	Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation
title_fullStr	Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation
title_full_unstemmed	Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation
title_sort	pyrophosphate-dependent atp formation from acetyl coenzyme a in <named-content content-type="genus-species">syntrophus aciditrophicus</named-content>, a new twist on atp formation
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/d1dab5dbda50462a851bf92528d0875e
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Pyrophosphate-Dependent ATP Formation from Acetyl Coenzyme A in <named-content content-type="genus-species">Syntrophus aciditrophicus</named-content>, a New Twist on ATP Formation

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