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Title: Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1

Abstract

Bacteria increase their metabolic capacity via the acquisition of genetic material or by the mutation of genes already present in the genome. Here, we explore the mechanisms and trade-offs involved whenShewanella oneidensis, a bacterium that typically consumes small organic and amino acids, rapidly evolves to expand its metabolic capacity to catabolize glucose after a short period of adaptation to a glucose-rich environment. Using whole-genome sequencing and genetic approaches, we discovered that deletions in a region including the transcriptional repressor (nagR) that regulates the expression of genes associated with catabolism ofN-acetylglucosamine are the common basis for evolved glucose metabolism across populations. The loss ofnagRresults in the constitutive expression of genes for anN-acetylglucosamine permease (nagP) and kinase (nagK). We demonstrate that promiscuous activities of both NagP and NagK toward glucose allow for the transport and phosphorylation of glucose to glucose-6-phosphate, the initial events of glycolysis otherwise thought to be absent inS. oneidensis. 13C-based metabolic flux analysis uncovered that subsequent utilization was mediated by the Entner-Doudoroff pathway. This is an example whereby gene loss and preexisting enzymatic promiscuity, and not gain-of-function mutations, were the drivers of increased metabolic capacity. However, we observed a significant decrease in the growth rate on lactate after adaptationmore » to glucose catabolism, suggesting that trade-offs may explain why glycolytic function may not be readily observed inS. oneidensisin natural environments despite it being readily accessible through just a single mutational event.Gains in metabolic capacity are frequently associated with the acquisition of novel genetic material via natural or engineered horizontal gene transfer events. Here, we explored how a bacterium that typically consumes small organic acids and amino acids expands its metabolic capacity to include glucose via a loss of genetic material, a process frequently associated with a deterioration of metabolic function. Our findings highlight how the natural promiscuity of transporters and enzymes can be a key driver in expanding metabolic diversity and that many bacteria may possess a latent metabolic capacity accessible through one or a few mutations that remove regulatory functions. Our discovery of trade-offs between growth on lactate and on glucose suggests why this easily gained trait is not observed in nature.« less

Authors:
ORCiD logo [1];  [2]
  1. Univ. of Missouri, Columbia, MO (United States); Harvard Univ., Cambridge, MA (United States)
  2. Harvard Univ., Cambridge, MA (United States); Univ. of Idaho, Moscow, ID (United States)
Publication Date:
Research Org.:
Harvard Univ., Cambridge, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1425453
Grant/Contract Number:  
SC0006739
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Volume: 199; Journal Issue: 11; Journal ID: ISSN 0021-9193
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Chubiz, Lon M., and Marx, Christopher J. Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1. United States: N. p., 2017. Web. doi:10.1128/JB.00827-16.
Chubiz, Lon M., & Marx, Christopher J. Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1. United States. doi:10.1128/JB.00827-16.
Chubiz, Lon M., and Marx, Christopher J. Mon . "Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1". United States. doi:10.1128/JB.00827-16. https://www.osti.gov/servlets/purl/1425453.
@article{osti_1425453,
title = {Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1},
author = {Chubiz, Lon M. and Marx, Christopher J.},
abstractNote = {Bacteria increase their metabolic capacity via the acquisition of genetic material or by the mutation of genes already present in the genome. Here, we explore the mechanisms and trade-offs involved whenShewanella oneidensis, a bacterium that typically consumes small organic and amino acids, rapidly evolves to expand its metabolic capacity to catabolize glucose after a short period of adaptation to a glucose-rich environment. Using whole-genome sequencing and genetic approaches, we discovered that deletions in a region including the transcriptional repressor (nagR) that regulates the expression of genes associated with catabolism ofN-acetylglucosamine are the common basis for evolved glucose metabolism across populations. The loss ofnagRresults in the constitutive expression of genes for anN-acetylglucosamine permease (nagP) and kinase (nagK). We demonstrate that promiscuous activities of both NagP and NagK toward glucose allow for the transport and phosphorylation of glucose to glucose-6-phosphate, the initial events of glycolysis otherwise thought to be absent inS. oneidensis.13C-based metabolic flux analysis uncovered that subsequent utilization was mediated by the Entner-Doudoroff pathway. This is an example whereby gene loss and preexisting enzymatic promiscuity, and not gain-of-function mutations, were the drivers of increased metabolic capacity. However, we observed a significant decrease in the growth rate on lactate after adaptation to glucose catabolism, suggesting that trade-offs may explain why glycolytic function may not be readily observed inS. oneidensisin natural environments despite it being readily accessible through just a single mutational event.Gains in metabolic capacity are frequently associated with the acquisition of novel genetic material via natural or engineered horizontal gene transfer events. Here, we explored how a bacterium that typically consumes small organic acids and amino acids expands its metabolic capacity to include glucose via a loss of genetic material, a process frequently associated with a deterioration of metabolic function. Our findings highlight how the natural promiscuity of transporters and enzymes can be a key driver in expanding metabolic diversity and that many bacteria may possess a latent metabolic capacity accessible through one or a few mutations that remove regulatory functions. Our discovery of trade-offs between growth on lactate and on glucose suggests why this easily gained trait is not observed in nature.},
doi = {10.1128/JB.00827-16},
journal = {Journal of Bacteriology},
number = 11,
volume = 199,
place = {United States},
year = {Mon Mar 13 00:00:00 EDT 2017},
month = {Mon Mar 13 00:00:00 EDT 2017}
}

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