title: A Genome-Scale Model ofShewanella piezotoleransSimulates Mechanisms of Metabolic Diversity and Energy Conservation.
abstract: Shewanella piezotoleransstrain WP3 belongs to the group 1 branch of theShewanellagenus 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 2Shewanellaspecies. 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 otherShewanellaspecies. 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 oneidensisMR-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.IMPORTANCEThe well-studied nature of the metabolic diversity ofShewanellabacteria makes species from this genus a promising platform for investigating the evolution of carbon metabolism and energy conservation. TheShewanellaphylogeny 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 ofShewanella piezotoleransstrain WP3 represented the first model forShewanellagroup 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.
authors.affiliation: Department of Cell and Molecular Biology, College of the Environment and Life Sciences, University of Rhode Island, Kingston, Rhode Island, USA; Graduate School of Biological and Environmental Sciences, College of the Environment and Life Sciences, University of Rhode Island, Kingston, Rhode Island, USA.
authors.forename: Keith
authors.initials: K
authors.lastname: Dufault-Thompson
authors.affiliation: State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, People's Republic of China.
authors.forename: Huahua
authors.initials: H
authors.lastname: Jian
authors.affiliation: State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, People's Republic of China.
authors.forename: Ruixue
authors.initials: R
authors.lastname: Cheng
authors.affiliation: State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, People's Republic of China.
authors.forename: Jiefu
authors.initials: J
authors.lastname: Li
authors.affiliation: State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, People's Republic of China.
authors.forename: Fengping
authors.initials: F
authors.lastname: Wang
authors.affiliation: Department of Cell and Molecular Biology, College of the Environment and Life Sciences, University of Rhode Island, Kingston, Rhode Island, USA.
authors.forename: Ying
authors.identifier: 0000-0001-8759-0194
authors.initials: Y
authors.lastname: Zhang
keywords: Shewanella; metabolic modeling