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Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1
- Source :
- Journal of Bacteriology
- Publication Year :
- 2017
- Publisher :
- American Society for Microbiology, 2017.
-
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.
- Subjects :
- 0301 basic medicine
Shewanella
Monosaccharide Transport Proteins
substrate promiscuity
030106 microbiology
medicine.disease_cause
Microbiology
Acetylglucosamine
03 medical and health sciences
Bacterial Proteins
Metabolic flux analysis
metabolic capacity
medicine
Glycolysis
Shewanella oneidensis
Molecular Biology
Gene
Regulation of gene expression
Mutation
biology
Catabolism
adaptive mutations
Gene Expression Regulation, Bacterial
Metabolism
glycolysis
biology.organism_classification
Cell biology
Glucose
trade-offs
030104 developmental biology
Biochemistry
Research Article
Subjects
Details
- ISSN :
- 10985530 and 00219193
- Volume :
- 199
- Database :
- OpenAIRE
- Journal :
- Journal of Bacteriology
- Accession number :
- edsair.doi.dedup.....41a4176e8f8c902b7141744bd17ad8a9