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Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies
The ability to successfully adapt to changing host conditions is crucial for full virulence of bacterial pathogens. Staphylococcus aureus has to cope with fluctuating oxygen concentrations during the course of infection. Hence, we studied the effect of oxygen on glucose metabolism in non-growing S....
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2013
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3589339/ https://www.ncbi.nlm.nih.gov/pubmed/23472168 http://dx.doi.org/10.1371/journal.pone.0058277 |
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author | Ferreira, Maria Teresa Manso, Ana S. Gaspar, Paula Pinho, Mariana G. Neves, Ana Rute |
author_facet | Ferreira, Maria Teresa Manso, Ana S. Gaspar, Paula Pinho, Mariana G. Neves, Ana Rute |
author_sort | Ferreira, Maria Teresa |
collection | PubMed |
description | The ability to successfully adapt to changing host conditions is crucial for full virulence of bacterial pathogens. Staphylococcus aureus has to cope with fluctuating oxygen concentrations during the course of infection. Hence, we studied the effect of oxygen on glucose metabolism in non-growing S. aureus COL-S cells by in vivo (13)C-NMR. Glucose catabolism was probed at different oxygen concentrations in suspensions of cells grown aerobically (direct effects on metabolism) or anaerobically (transcriptional adjustment to oxygen deprivation). In aerobically-grown cells, the rate of glucose consumption diminished progressively with decreasing oxygen concentrations. Additionally, oxygen deprivation resulted in biphasic glucose consumption, with the second phase presenting a higher rate. The fructose-1,6-bisphosphate pool peaked while glucose was still abundant, but the transient maximum varied with the oxygen concentration. As oxygen became limiting mannitol/mannitol-1-phosphate were detected as products of glucose catabolism. Under anoxic conditions, accumulation of mannitol-1-phosphate ceased with the switch to higher glucose consumption rates, which implies the activation of a more efficient means by which NAD(+) can be regenerated. The distribution of end-products deriving from glucose catabolism was dramatically affected by oxygen: acetate increased and lactate decreased with the oxygen concentration; ethanol was formed only anaerobically. Moreover, oxygen promoted the energetically favourable conversion of lactate into acetate, which was particularly noticeable under fully oxygenated conditions. Interestingly, under aerobiosis growing S. aureus cells also converted lactate to acetate, used simultaneously glucose and lactate as substrates for growth, and grew considerably well on lactate-medium. We propose that the efficient lactate catabolism may endow S. aureus with a metabolic advantage in its ecological niche. |
format | Online Article Text |
id | pubmed-3589339 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2013 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-35893392013-03-07 Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies Ferreira, Maria Teresa Manso, Ana S. Gaspar, Paula Pinho, Mariana G. Neves, Ana Rute PLoS One Research Article The ability to successfully adapt to changing host conditions is crucial for full virulence of bacterial pathogens. Staphylococcus aureus has to cope with fluctuating oxygen concentrations during the course of infection. Hence, we studied the effect of oxygen on glucose metabolism in non-growing S. aureus COL-S cells by in vivo (13)C-NMR. Glucose catabolism was probed at different oxygen concentrations in suspensions of cells grown aerobically (direct effects on metabolism) or anaerobically (transcriptional adjustment to oxygen deprivation). In aerobically-grown cells, the rate of glucose consumption diminished progressively with decreasing oxygen concentrations. Additionally, oxygen deprivation resulted in biphasic glucose consumption, with the second phase presenting a higher rate. The fructose-1,6-bisphosphate pool peaked while glucose was still abundant, but the transient maximum varied with the oxygen concentration. As oxygen became limiting mannitol/mannitol-1-phosphate were detected as products of glucose catabolism. Under anoxic conditions, accumulation of mannitol-1-phosphate ceased with the switch to higher glucose consumption rates, which implies the activation of a more efficient means by which NAD(+) can be regenerated. The distribution of end-products deriving from glucose catabolism was dramatically affected by oxygen: acetate increased and lactate decreased with the oxygen concentration; ethanol was formed only anaerobically. Moreover, oxygen promoted the energetically favourable conversion of lactate into acetate, which was particularly noticeable under fully oxygenated conditions. Interestingly, under aerobiosis growing S. aureus cells also converted lactate to acetate, used simultaneously glucose and lactate as substrates for growth, and grew considerably well on lactate-medium. We propose that the efficient lactate catabolism may endow S. aureus with a metabolic advantage in its ecological niche. Public Library of Science 2013-03-05 /pmc/articles/PMC3589339/ /pubmed/23472168 http://dx.doi.org/10.1371/journal.pone.0058277 Text en © 2013 Ferreira et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Ferreira, Maria Teresa Manso, Ana S. Gaspar, Paula Pinho, Mariana G. Neves, Ana Rute Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies |
title | Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies |
title_full | Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies |
title_fullStr | Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies |
title_full_unstemmed | Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies |
title_short | Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies |
title_sort | effect of oxygen on glucose metabolism: utilization of lactate in staphylococcus aureus as revealed by in vivo nmr studies |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3589339/ https://www.ncbi.nlm.nih.gov/pubmed/23472168 http://dx.doi.org/10.1371/journal.pone.0058277 |
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