Growth Trade-Offs Accompany the Emergence of Glycolytic Metabolism in Shewanella oneidensis MR-1 [electronic resource].
- Washington, D.C. : United States. Dept. of Energy. Office of Science, 2017. and Oak Ridge, Tenn. : Distributed by the Office of Scientific and Technical Information, U.S. Dept. of Energy
- Physical Description:
- Article numbers e00,827-16 : digital, PDF file
- Additional Creators:
- Harvard University, United States. Department of Energy. Office of Science, and United States. Department of Energy. Office of Scientific and Technical Information
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- Free-to-read Unrestricted online access
- 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<named-content content-type='genus-species'>Shewanella oneidensis</named-content>, 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 (<italic>nagR</italic>) that regulates the expression of genes associated with catabolism of<italic>N</italic>-acetylglucosamine are the common basis for evolved glucose metabolism across populations. The loss of<italic>nagR</italic>results in the constitutive expression of genes for an<italic>N</italic>-acetylglucosamine permease (<italic>nagP</italic>) and kinase (<italic>nagK</italic>). 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<named-content content-type='genus-species'>S. oneidensis</named-content>.<sup>13</sup>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<named-content content-type='genus-species'>S. oneidensis</named-content>in 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.
- Published through SciTech Connect., 03/13/2017., Journal of Bacteriology 199 11 ISSN 0021-9193 AM, and Lon M. Chubiz; Christopher J. Marx.
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