Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation

ABSTRACT In this work, a systematic methodology was developed (based on known biochemistry, physiology, and bioenergetics) for the automated feasibility evaluation and net ATP yield quantification of large sets of pathway variants. Possible pathway variants differ in their intermediate metabolites,...

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Autores principales:	Mauricio Patón, Héctor H. Hernández, Jorge Rodríguez
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	bioenergetics modeling metabolic pathway modeling metabolic energy conservation interspecies electron transfer Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f3271370a1ae40ef9842370fe3c119d5
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spelling	oai:doaj.org-article:f3271370a1ae40ef9842370fe3c119d52021-12-02T18:44:44ZComprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation10.1128/mSystems.00814-202379-5077https://doaj.org/article/f3271370a1ae40ef9842370fe3c119d52020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00814-20https://doaj.org/toc/2379-5077ABSTRACT In this work, a systematic methodology was developed (based on known biochemistry, physiology, and bioenergetics) for the automated feasibility evaluation and net ATP yield quantification of large sets of pathway variants. Possible pathway variants differ in their intermediate metabolites, in which electron carriers are involved, in which steps are consuming/producing ATP, and in which steps are coupled to (and to how many) proton (or its equivalent) translocations. A pathway variant is deemed feasible, under a given set of physiological and environmental conditions, only if all pathway reaction steps have nonpositive Gibbs energy changes and if all the metabolite concentrations remain within an acceptable physiological range (10−6 to 10−2 M). The complete understanding of syntrophic propionate oxidation remains elusive due to uncertainties in pathways and the mechanisms for interspecies electron transfer (IET). Several million combinations of pathway variants and parameters/conditions were evaluated for propionate oxidation, providing unprecedented mechanistic insight into its biochemical and bioenergetic landscape. Our results show that, under a scenario of optimum environmental conditions for propionate oxidation, the Smithella pathway yields the most ATP and the methylmalonyl-coenzyme A (CoA) pathways can generate sufficient ATP for growth only under a cyclical pathway configuration with pyruvate. The results under conditions typical of methanogenic environments show that propionate oxidation via the lactate and via the hydroxypropionyl-CoA pathways yield the most ATP. IET between propionate oxidizers and methanogens can proceed either by dissolved hydrogen via the Smithella pathway or by different mechanisms (e.g., formate or direct IET) if other pathways are used. IMPORTANCE In this work, an original methodology was developed that quantifies bioenergetically and physiologically feasible net ATP yields for large numbers of microbial metabolic pathways and their variants under different conditions. All variants are evaluated, which ensures global optimality in finding the pathway variant(s) leading to the highest ATP yield. The methodology is designed to be especially relevant to hypothesize on which microbial pathway variants should be most favored in microbial ecosystems under high selective pressure for efficient metabolic energy conservation. Syntrophic microbial oxidation of propionate to acetate has an extremely small quantity of available energy and requires an extremely high metabolic efficiency to sustain life. Our results bring mechanistic insights into the optimum pathway variants, other metabolic bottlenecks, and the impact of environmental conditions on the ATP yields. Additionally, our results conclude that, as previously reported, under specific conditions, IET mechanisms other than hydrogen must exist to simultaneously sustain the growth of both propionate oxidizers and hydrogenotrophic methanogens.Mauricio PatónHéctor H. HernándezJorge RodríguezAmerican Society for Microbiologyarticlebioenergetics modelingmetabolic pathway modelingmetabolic energy conservationinterspecies electron transferMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	bioenergetics modeling metabolic pathway modeling metabolic energy conservation interspecies electron transfer Microbiology QR1-502
spellingShingle	bioenergetics modeling metabolic pathway modeling metabolic energy conservation interspecies electron transfer Microbiology QR1-502 Mauricio Patón Héctor H. Hernández Jorge Rodríguez Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation
description	ABSTRACT In this work, a systematic methodology was developed (based on known biochemistry, physiology, and bioenergetics) for the automated feasibility evaluation and net ATP yield quantification of large sets of pathway variants. Possible pathway variants differ in their intermediate metabolites, in which electron carriers are involved, in which steps are consuming/producing ATP, and in which steps are coupled to (and to how many) proton (or its equivalent) translocations. A pathway variant is deemed feasible, under a given set of physiological and environmental conditions, only if all pathway reaction steps have nonpositive Gibbs energy changes and if all the metabolite concentrations remain within an acceptable physiological range (10−6 to 10−2 M). The complete understanding of syntrophic propionate oxidation remains elusive due to uncertainties in pathways and the mechanisms for interspecies electron transfer (IET). Several million combinations of pathway variants and parameters/conditions were evaluated for propionate oxidation, providing unprecedented mechanistic insight into its biochemical and bioenergetic landscape. Our results show that, under a scenario of optimum environmental conditions for propionate oxidation, the Smithella pathway yields the most ATP and the methylmalonyl-coenzyme A (CoA) pathways can generate sufficient ATP for growth only under a cyclical pathway configuration with pyruvate. The results under conditions typical of methanogenic environments show that propionate oxidation via the lactate and via the hydroxypropionyl-CoA pathways yield the most ATP. IET between propionate oxidizers and methanogens can proceed either by dissolved hydrogen via the Smithella pathway or by different mechanisms (e.g., formate or direct IET) if other pathways are used. IMPORTANCE In this work, an original methodology was developed that quantifies bioenergetically and physiologically feasible net ATP yields for large numbers of microbial metabolic pathways and their variants under different conditions. All variants are evaluated, which ensures global optimality in finding the pathway variant(s) leading to the highest ATP yield. The methodology is designed to be especially relevant to hypothesize on which microbial pathway variants should be most favored in microbial ecosystems under high selective pressure for efficient metabolic energy conservation. Syntrophic microbial oxidation of propionate to acetate has an extremely small quantity of available energy and requires an extremely high metabolic efficiency to sustain life. Our results bring mechanistic insights into the optimum pathway variants, other metabolic bottlenecks, and the impact of environmental conditions on the ATP yields. Additionally, our results conclude that, as previously reported, under specific conditions, IET mechanisms other than hydrogen must exist to simultaneously sustain the growth of both propionate oxidizers and hydrogenotrophic methanogens.
format	article
author	Mauricio Patón Héctor H. Hernández Jorge Rodríguez
author_facet	Mauricio Patón Héctor H. Hernández Jorge Rodríguez
author_sort	Mauricio Patón
title	Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation
title_short	Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation
title_full	Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation
title_fullStr	Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation
title_full_unstemmed	Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation
title_sort	comprehensive bioenergetic evaluation of microbial pathway variants in syntrophic propionate oxidation
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/f3271370a1ae40ef9842370fe3c119d5
work_keys_str_mv	AT mauriciopaton comprehensivebioenergeticevaluationofmicrobialpathwayvariantsinsyntrophicpropionateoxidation AT hectorhhernandez comprehensivebioenergeticevaluationofmicrobialpathwayvariantsinsyntrophicpropionateoxidation AT jorgerodriguez comprehensivebioenergeticevaluationofmicrobialpathwayvariantsinsyntrophicpropionateoxidation
_version_	1718377715923419136

Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation

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