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

Abstract

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 when Shewanella 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 of N -acetylglucosamine are the common basis for evolved glucose metabolism across populations. The loss of nagR results in the constitutive expression of genes for an N -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 in S. oneidensis . 13 C-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 driversmore » 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 in S. oneidensis in natural environments despite it being readily accessible through just a single mutational event. IMPORTANCE 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. Department of Biology, University of Missouri—St. Louis, St. Louis, Missouri, USA, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA
  2. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA, Department of Biological Sciences, University of Idaho, Moscow, Idaho, USA, Center for Modeling Complex Interactions, University of Idaho, Moscow, Idaho, USA, Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, Idaho, USA
Publication Date:
Research Org.:
Harvard Univ., Cambridge, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1658405
Alternate Identifier(s):
OSTI ID: 1425453
Grant/Contract Number:  
SC0006731; SC0006739
Resource Type:
Journal Article: Published Article
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Name: Journal of Bacteriology 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., Marx, Christopher J., and Becker, ed., Anke. 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., & Becker, ed., Anke. Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1. United States. https://doi.org/10.1128/JB.00827-16
Chubiz, Lon M., Marx, Christopher J., and Becker, ed., Anke. Thu . "Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1". United States. https://doi.org/10.1128/JB.00827-16.
@article{osti_1658405,
title = {Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1},
author = {Chubiz, Lon M. and Marx, Christopher J. and Becker, ed., Anke},
abstractNote = {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 when Shewanella 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 of N -acetylglucosamine are the common basis for evolved glucose metabolism across populations. The loss of nagR results in the constitutive expression of genes for an N -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 in S. oneidensis . 13 C-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 in S. oneidensis in natural environments despite it being readily accessible through just a single mutational event. IMPORTANCE 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},
url = {https://www.osti.gov/biblio/1658405}, journal = {Journal of Bacteriology},
issn = {0021-9193},
number = 11,
volume = 199,
place = {United States},
year = {2017},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.1128/JB.00827-16

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Cited by: 3 works
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