A Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation

ABSTRACT Shewanella piezotolerans strain WP3 belongs to the group 1 branch of the Shewanella genus and is a piezotolerant and psychrotolerant species isolated from the deep sea. In this study, a genome-scale model was constructed for WP3 using a combination of genome annotation, ortholog mapping, an...

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Autores principales:	Keith Dufault-Thompson, Huahua Jian, Ruixue Cheng, Jiefu Li, Fengping Wang, Ying Zhang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Shewanella metabolic modeling Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/480631d814b04f59b03b49652b4c008e
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spelling	oai:doaj.org-article:480631d814b04f59b03b49652b4c008e2021-12-02T19:48:49ZA Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation10.1128/mSystems.00165-162379-5077https://doaj.org/article/480631d814b04f59b03b49652b4c008e2017-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00165-16https://doaj.org/toc/2379-5077ABSTRACT Shewanella piezotolerans strain WP3 belongs to the group 1 branch of the Shewanella genus and is a piezotolerant and psychrotolerant species isolated from the deep sea. In this study, a genome-scale model was constructed for WP3 using a combination of genome annotation, ortholog mapping, and physiological verification. The metabolic reconstruction contained 806 genes, 653 metabolites, and 922 reactions, including central metabolic functions that represented nonhomologous replacements between the group 1 and group 2 Shewanella species. Metabolic simulations with the WP3 model demonstrated consistency with existing knowledge about the physiology of the organism. A comparison of model simulations with experimental measurements verified the predicted growth profiles under increasing concentrations of carbon sources. The WP3 model was applied to study mechanisms of anaerobic respiration through investigating energy conservation, redox balancing, and the generation of proton motive force. Despite being an obligate respiratory organism, WP3 was predicted to use substrate-level phosphorylation as the primary source of energy conservation under anaerobic conditions, a trait previously identified in other Shewanella species. Further investigation of the ATP synthase activity revealed a positive correlation between the availability of reducing equivalents in the cell and the directionality of the ATP synthase reaction flux. Comparison of the WP3 model with an existing model of a group 2 species, Shewanella oneidensis MR-1, revealed that the WP3 model demonstrated greater flexibility in ATP production under the anaerobic conditions. Such flexibility could be advantageous to WP3 for its adaptation to fluctuating availability of organic carbon sources in the deep sea. IMPORTANCE The well-studied nature of the metabolic diversity of Shewanella bacteria makes species from this genus a promising platform for investigating the evolution of carbon metabolism and energy conservation. The Shewanella phylogeny is diverged into two major branches, referred to as group 1 and group 2. While the genotype-phenotype connections of group 2 species have been extensively studied with metabolic modeling, a genome-scale model has been missing for the group 1 species. The metabolic reconstruction of Shewanella piezotolerans strain WP3 represented the first model for Shewanella group 1 and the first model among piezotolerant and psychrotolerant deep-sea bacteria. The model brought insights into the mechanisms of energy conservation in WP3 under anaerobic conditions and highlighted its metabolic flexibility in using diverse carbon sources. Overall, the model opens up new opportunities for investigating energy conservation and metabolic adaptation, and it provides a prototype for systems-level modeling of other deep-sea microorganisms.Keith Dufault-ThompsonHuahua JianRuixue ChengJiefu LiFengping WangYing ZhangAmerican Society for MicrobiologyarticleShewanellametabolic modelingMicrobiologyQR1-502ENmSystems, Vol 2, Iss 2 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Shewanella metabolic modeling Microbiology QR1-502
spellingShingle	Shewanella metabolic modeling Microbiology QR1-502 Keith Dufault-Thompson Huahua Jian Ruixue Cheng Jiefu Li Fengping Wang Ying Zhang A Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation
description	ABSTRACT Shewanella piezotolerans strain WP3 belongs to the group 1 branch of the Shewanella genus and is a piezotolerant and psychrotolerant species isolated from the deep sea. In this study, a genome-scale model was constructed for WP3 using a combination of genome annotation, ortholog mapping, and physiological verification. The metabolic reconstruction contained 806 genes, 653 metabolites, and 922 reactions, including central metabolic functions that represented nonhomologous replacements between the group 1 and group 2 Shewanella species. Metabolic simulations with the WP3 model demonstrated consistency with existing knowledge about the physiology of the organism. A comparison of model simulations with experimental measurements verified the predicted growth profiles under increasing concentrations of carbon sources. The WP3 model was applied to study mechanisms of anaerobic respiration through investigating energy conservation, redox balancing, and the generation of proton motive force. Despite being an obligate respiratory organism, WP3 was predicted to use substrate-level phosphorylation as the primary source of energy conservation under anaerobic conditions, a trait previously identified in other Shewanella species. Further investigation of the ATP synthase activity revealed a positive correlation between the availability of reducing equivalents in the cell and the directionality of the ATP synthase reaction flux. Comparison of the WP3 model with an existing model of a group 2 species, Shewanella oneidensis MR-1, revealed that the WP3 model demonstrated greater flexibility in ATP production under the anaerobic conditions. Such flexibility could be advantageous to WP3 for its adaptation to fluctuating availability of organic carbon sources in the deep sea. IMPORTANCE The well-studied nature of the metabolic diversity of Shewanella bacteria makes species from this genus a promising platform for investigating the evolution of carbon metabolism and energy conservation. The Shewanella phylogeny is diverged into two major branches, referred to as group 1 and group 2. While the genotype-phenotype connections of group 2 species have been extensively studied with metabolic modeling, a genome-scale model has been missing for the group 1 species. The metabolic reconstruction of Shewanella piezotolerans strain WP3 represented the first model for Shewanella group 1 and the first model among piezotolerant and psychrotolerant deep-sea bacteria. The model brought insights into the mechanisms of energy conservation in WP3 under anaerobic conditions and highlighted its metabolic flexibility in using diverse carbon sources. Overall, the model opens up new opportunities for investigating energy conservation and metabolic adaptation, and it provides a prototype for systems-level modeling of other deep-sea microorganisms.
format	article
author	Keith Dufault-Thompson Huahua Jian Ruixue Cheng Jiefu Li Fengping Wang Ying Zhang
author_facet	Keith Dufault-Thompson Huahua Jian Ruixue Cheng Jiefu Li Fengping Wang Ying Zhang
author_sort	Keith Dufault-Thompson
title	A Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation
title_short	A Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation
title_full	A Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation
title_fullStr	A Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation
title_full_unstemmed	A Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation
title_sort	genome-scale model of <italic toggle="yes">shewanella piezotolerans</italic> simulates mechanisms of metabolic diversity and energy conservation
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/480631d814b04f59b03b49652b4c008e
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A Genome-Scale Model of <italic toggle="yes">Shewanella piezotolerans</italic> Simulates Mechanisms of Metabolic Diversity and Energy Conservation

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