A Genome-Scale Model of Shewanella piezotolerans Simulates Mechanisms of Metabolic Diversity and Energy Conservation

Abstract

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.

Reconstruction and analysis of thermodynamically-constrained models reveal metabolic responses of a deep-sea bacterium to temperature perturbations

“…The ATPS4r reaction, when carrying non-zero fluxes, was predicted to run only in the ATP-consuming, proton-pumping direction ( Fig. 3 ), similar to what has been observed in other Shewanella species (34, 65). The lack of ATPS4r flux in the 4°C model likely reflects a mechanism of ATP conservation.…”

“…Inoculations of three biological replicates for each growth temperature (4°C, 15°C, and 20°C) were performed in 150 mL of fresh LMO-812 media (34) with 1 mL of inoculum obtained from cultures grown to exponential phase at the optimal temperature (15°C) in 2216 Marine Medium (Difco). The cultures were grown with 5 mM GlcNac as the sole carbon source in aerobic conditions at each temperature with shaking, and an initial OD 600 of 0.002 was measured for each inoculation.…”

“…WP2 has an optimal growth temperature of 10–15°C, a growth range of 0–20°C, and exhibits the hallmark metabolic versatility seen in the Shewanella genus (32, 33). WP2 belongs to the Group 1 Shewanella , a clade mainly consisting of deep-sea strains characterized by their tolerance and adaptation to low-temperature and high-pressure conditions (34, 35). WP2 represents a distinct clade that is distant from two other Group 1 Shewanella strains that have been represented using Genome-scale models (GEMs): Shewanella loihica PV-4 and S. piezotolerans WP3 (34, 36).…”

“…WP2 belongs to the Group 1 Shewanella , a clade mainly consisting of deep-sea strains characterized by their tolerance and adaptation to low-temperature and high-pressure conditions (34, 35). WP2 represents a distinct clade that is distant from two other Group 1 Shewanella strains that have been represented using Genome-scale models (GEMs): Shewanella loihica PV-4 and S. piezotolerans WP3 (34, 36). An analysis of the complete genome of WP2 revealed an expansion of transposable elements, motility genes, and chemotaxis genes compared to other deep-sea Shewanella (37).…”

FindPrimaryPairs: An efficient algorithm for predicting element-transferring reactant/product pairs in metabolic networks

“…It comprises transformations of metabolites through biochemical reactions and can be viewed as a network graph, where metabolites are represented as individual vertices and reactions are represented as edges connecting the vertices. The reconstruction of metabolic networks can be applied to targeted pathways, species specific genome-scale models (GEMs) [ 1 , 2 ], or to represent an ensemble of metabolic potentials from all organisms [ 3 ]. In any case, metabolic reconstructions can quickly result in complex network topologies even for representing individual pathways in the central metabolism.…”