Within-host evolution of Staphylococcus aureus during asymptomatic carriage.
<h4>Background</h4>Staphylococcus aureus is a major cause of healthcare associated mortality, but like many important bacterial pathogens, it is a common constituent of the normal human body flora. Around a third of healthy adults are carriers. Recent evidence suggests that evolution of...
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2013
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oai:doaj.org-article:ceaa09b68e7541248844928c570fc9422021-11-18T07:47:09ZWithin-host evolution of Staphylococcus aureus during asymptomatic carriage.1932-620310.1371/journal.pone.0061319https://doaj.org/article/ceaa09b68e7541248844928c570fc9422013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23658690/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Staphylococcus aureus is a major cause of healthcare associated mortality, but like many important bacterial pathogens, it is a common constituent of the normal human body flora. Around a third of healthy adults are carriers. Recent evidence suggests that evolution of S. aureus during nasal carriage may be associated with progression to invasive disease. However, a more detailed understanding of within-host evolution under natural conditions is required to appreciate the evolutionary and mechanistic reasons why commensal bacteria such as S. aureus cause disease. Therefore we examined in detail the evolutionary dynamics of normal, asymptomatic carriage. Sequencing a total of 131 genomes across 13 singly colonized hosts using the Illumina platform, we investigated diversity, selection, population dynamics and transmission during the short-term evolution of S. aureus.<h4>Principal findings</h4>We characterized the processes by which the raw material for evolution is generated: micro-mutation (point mutation and small insertions/deletions), macro-mutation (large insertions/deletions) and the loss or acquisition of mobile elements (plasmids and bacteriophages). Through an analysis of synonymous, non-synonymous and intergenic mutations we discovered a fitness landscape dominated by purifying selection, with rare examples of adaptive change in genes encoding surface-anchored proteins and an enterotoxin. We found evidence for dramatic, hundred-fold fluctuations in the size of the within-host population over time, which we related to the cycle of colonization and clearance. Using a newly-developed population genetics approach to detect recent transmission among hosts, we revealed evidence for recent transmission between some of our subjects, including a husband and wife both carrying populations of methicillin-resistant S. aureus (MRSA).<h4>Significance</h4>This investigation begins to paint a picture of the within-host evolution of an important bacterial pathogen during its prevailing natural state, asymptomatic carriage. These results also have wider significance as a benchmark for future systematic studies of evolution during invasive S. aureus disease.Tanya GolubchikElizabeth M BattyRuth R MillerHelen FarrBernadette C YoungHanna Larner-SvenssonRowena FungHeather GodwinKyle KnoxAntonina VotintsevaRichard G EverittTeresa StreetMadeleine CuleCamilla L C IpXavier DidelotTimothy E A PetoRosalind M HardingDaniel J WilsonDerrick W CrookRory BowdenPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 5, p e61319 (2013) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Medicine R Science Q |
| spellingShingle |
Medicine R Science Q Tanya Golubchik Elizabeth M Batty Ruth R Miller Helen Farr Bernadette C Young Hanna Larner-Svensson Rowena Fung Heather Godwin Kyle Knox Antonina Votintseva Richard G Everitt Teresa Street Madeleine Cule Camilla L C Ip Xavier Didelot Timothy E A Peto Rosalind M Harding Daniel J Wilson Derrick W Crook Rory Bowden Within-host evolution of Staphylococcus aureus during asymptomatic carriage. |
| description |
<h4>Background</h4>Staphylococcus aureus is a major cause of healthcare associated mortality, but like many important bacterial pathogens, it is a common constituent of the normal human body flora. Around a third of healthy adults are carriers. Recent evidence suggests that evolution of S. aureus during nasal carriage may be associated with progression to invasive disease. However, a more detailed understanding of within-host evolution under natural conditions is required to appreciate the evolutionary and mechanistic reasons why commensal bacteria such as S. aureus cause disease. Therefore we examined in detail the evolutionary dynamics of normal, asymptomatic carriage. Sequencing a total of 131 genomes across 13 singly colonized hosts using the Illumina platform, we investigated diversity, selection, population dynamics and transmission during the short-term evolution of S. aureus.<h4>Principal findings</h4>We characterized the processes by which the raw material for evolution is generated: micro-mutation (point mutation and small insertions/deletions), macro-mutation (large insertions/deletions) and the loss or acquisition of mobile elements (plasmids and bacteriophages). Through an analysis of synonymous, non-synonymous and intergenic mutations we discovered a fitness landscape dominated by purifying selection, with rare examples of adaptive change in genes encoding surface-anchored proteins and an enterotoxin. We found evidence for dramatic, hundred-fold fluctuations in the size of the within-host population over time, which we related to the cycle of colonization and clearance. Using a newly-developed population genetics approach to detect recent transmission among hosts, we revealed evidence for recent transmission between some of our subjects, including a husband and wife both carrying populations of methicillin-resistant S. aureus (MRSA).<h4>Significance</h4>This investigation begins to paint a picture of the within-host evolution of an important bacterial pathogen during its prevailing natural state, asymptomatic carriage. These results also have wider significance as a benchmark for future systematic studies of evolution during invasive S. aureus disease. |
| format |
article |
| author |
Tanya Golubchik Elizabeth M Batty Ruth R Miller Helen Farr Bernadette C Young Hanna Larner-Svensson Rowena Fung Heather Godwin Kyle Knox Antonina Votintseva Richard G Everitt Teresa Street Madeleine Cule Camilla L C Ip Xavier Didelot Timothy E A Peto Rosalind M Harding Daniel J Wilson Derrick W Crook Rory Bowden |
| author_facet |
Tanya Golubchik Elizabeth M Batty Ruth R Miller Helen Farr Bernadette C Young Hanna Larner-Svensson Rowena Fung Heather Godwin Kyle Knox Antonina Votintseva Richard G Everitt Teresa Street Madeleine Cule Camilla L C Ip Xavier Didelot Timothy E A Peto Rosalind M Harding Daniel J Wilson Derrick W Crook Rory Bowden |
| author_sort |
Tanya Golubchik |
| title |
Within-host evolution of Staphylococcus aureus during asymptomatic carriage. |
| title_short |
Within-host evolution of Staphylococcus aureus during asymptomatic carriage. |
| title_full |
Within-host evolution of Staphylococcus aureus during asymptomatic carriage. |
| title_fullStr |
Within-host evolution of Staphylococcus aureus during asymptomatic carriage. |
| title_full_unstemmed |
Within-host evolution of Staphylococcus aureus during asymptomatic carriage. |
| title_sort |
within-host evolution of staphylococcus aureus during asymptomatic carriage. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2013 |
| url |
https://doaj.org/article/ceaa09b68e7541248844928c570fc942 |
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