Range Expansion and the Origin of USA300 North American Epidemic Methicillin-Resistant <italic toggle="yes">Staphylococcus aureus</italic>
ABSTRACT The USA300 North American epidemic (USA300-NAE) clone of methicillin-resistant Staphylococcus aureus has caused a wave of severe skin and soft tissue infections in the United States since it emerged in the early 2000s, but its geographic origin is obscure. Here we use the population genomic...
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American Society for Microbiology
2018
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oai:doaj.org-article:7f218b46d58048afa74e73d06b978a9f2021-11-15T15:53:25ZRange Expansion and the Origin of USA300 North American Epidemic Methicillin-Resistant <italic toggle="yes">Staphylococcus aureus</italic>10.1128/mBio.02016-172150-7511https://doaj.org/article/7f218b46d58048afa74e73d06b978a9f2018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02016-17https://doaj.org/toc/2150-7511ABSTRACT The USA300 North American epidemic (USA300-NAE) clone of methicillin-resistant Staphylococcus aureus has caused a wave of severe skin and soft tissue infections in the United States since it emerged in the early 2000s, but its geographic origin is obscure. Here we use the population genomic signatures expected from the serial founder effects of a geographic range expansion to infer the origin of USA300-NAE and identify polymorphisms associated with its spread. Genome sequences from 357 isolates from 22 U.S. states and territories and seven other countries are compared. We observe two significant signatures of range expansion, including decreases in genetic diversity and increases in derived allele frequency with geographic distance from the Pennsylvania region. These signatures account for approximately half of the core nucleotide variation of this clone, occur genome wide, and are robust to heterogeneity in temporal sampling of isolates, human population density, and recombination detection methods. The potential for positive selection of a gyrA fluoroquinolone resistance allele and several intergenic regions, along with a 2.4 times higher recombination rate in a resistant subclade, is noted. These results are the first to show a pattern of genetic variation that is consistent with a range expansion of an epidemic bacterial clone, and they highlight a rarely considered but potentially common mechanism by which genetic drift may profoundly influence bacterial genetic variation. IMPORTANCE The process of geographic spread of an origin population by a series of smaller populations can result in distinctive patterns of genetic variation. We detect these patterns for the first time with an epidemic bacterial clone and use them to uncover the clone’s geographic origin and variants associated with its spread. We study the USA300 clone of methicillin-resistant Staphylococcus aureus, which was first noticed in the early 2000s and subsequently became the leading cause of skin and soft tissue infections in the United States. The eastern United States is the most likely origin of epidemic USA300. Relatively few variants, which include an antibiotic resistance mutation, have persisted during this clone’s spread. Our study suggests that an early chapter in the genetic history of this epidemic bacterial clone was greatly influenced by random subsampling of isolates during the clone’s geographic spread.Lavanya ChallagundlaXiao LuoIsabella A. TicklerXavier DidelotDavid C. ColemanAnna C. ShoreGeoffrey W. CoombsDaniel O. SordelliEric L. BrownRobert SkovAnders Rhod LarsenJinnethe ReyesIraida E. RobledoGuillermo J. VazquezRaul RiveraPaul D. FeyKurt StevensonShu-Hua WangBarry N. KreiswirthJose R. MediavillaCesar A. AriasPaul J. PlanetRathel L. NolanFred C. TenoverRichard V. GoeringD. Ashley RobinsonAmerican Society for Microbiologyarticleepidemicsfluoroquinolonesfounder effectsgenetic driftpopulation geneticsrange expansionMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018) |
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epidemics fluoroquinolones founder effects genetic drift population genetics range expansion Microbiology QR1-502 |
| spellingShingle |
epidemics fluoroquinolones founder effects genetic drift population genetics range expansion Microbiology QR1-502 Lavanya Challagundla Xiao Luo Isabella A. Tickler Xavier Didelot David C. Coleman Anna C. Shore Geoffrey W. Coombs Daniel O. Sordelli Eric L. Brown Robert Skov Anders Rhod Larsen Jinnethe Reyes Iraida E. Robledo Guillermo J. Vazquez Raul Rivera Paul D. Fey Kurt Stevenson Shu-Hua Wang Barry N. Kreiswirth Jose R. Mediavilla Cesar A. Arias Paul J. Planet Rathel L. Nolan Fred C. Tenover Richard V. Goering D. Ashley Robinson Range Expansion and the Origin of USA300 North American Epidemic Methicillin-Resistant <italic toggle="yes">Staphylococcus aureus</italic> |
| description |
ABSTRACT The USA300 North American epidemic (USA300-NAE) clone of methicillin-resistant Staphylococcus aureus has caused a wave of severe skin and soft tissue infections in the United States since it emerged in the early 2000s, but its geographic origin is obscure. Here we use the population genomic signatures expected from the serial founder effects of a geographic range expansion to infer the origin of USA300-NAE and identify polymorphisms associated with its spread. Genome sequences from 357 isolates from 22 U.S. states and territories and seven other countries are compared. We observe two significant signatures of range expansion, including decreases in genetic diversity and increases in derived allele frequency with geographic distance from the Pennsylvania region. These signatures account for approximately half of the core nucleotide variation of this clone, occur genome wide, and are robust to heterogeneity in temporal sampling of isolates, human population density, and recombination detection methods. The potential for positive selection of a gyrA fluoroquinolone resistance allele and several intergenic regions, along with a 2.4 times higher recombination rate in a resistant subclade, is noted. These results are the first to show a pattern of genetic variation that is consistent with a range expansion of an epidemic bacterial clone, and they highlight a rarely considered but potentially common mechanism by which genetic drift may profoundly influence bacterial genetic variation. IMPORTANCE The process of geographic spread of an origin population by a series of smaller populations can result in distinctive patterns of genetic variation. We detect these patterns for the first time with an epidemic bacterial clone and use them to uncover the clone’s geographic origin and variants associated with its spread. We study the USA300 clone of methicillin-resistant Staphylococcus aureus, which was first noticed in the early 2000s and subsequently became the leading cause of skin and soft tissue infections in the United States. The eastern United States is the most likely origin of epidemic USA300. Relatively few variants, which include an antibiotic resistance mutation, have persisted during this clone’s spread. Our study suggests that an early chapter in the genetic history of this epidemic bacterial clone was greatly influenced by random subsampling of isolates during the clone’s geographic spread. |
| format |
article |
| author |
Lavanya Challagundla Xiao Luo Isabella A. Tickler Xavier Didelot David C. Coleman Anna C. Shore Geoffrey W. Coombs Daniel O. Sordelli Eric L. Brown Robert Skov Anders Rhod Larsen Jinnethe Reyes Iraida E. Robledo Guillermo J. Vazquez Raul Rivera Paul D. Fey Kurt Stevenson Shu-Hua Wang Barry N. Kreiswirth Jose R. Mediavilla Cesar A. Arias Paul J. Planet Rathel L. Nolan Fred C. Tenover Richard V. Goering D. Ashley Robinson |
| author_facet |
Lavanya Challagundla Xiao Luo Isabella A. Tickler Xavier Didelot David C. Coleman Anna C. Shore Geoffrey W. Coombs Daniel O. Sordelli Eric L. Brown Robert Skov Anders Rhod Larsen Jinnethe Reyes Iraida E. Robledo Guillermo J. Vazquez Raul Rivera Paul D. Fey Kurt Stevenson Shu-Hua Wang Barry N. Kreiswirth Jose R. Mediavilla Cesar A. Arias Paul J. Planet Rathel L. Nolan Fred C. Tenover Richard V. Goering D. Ashley Robinson |
| author_sort |
Lavanya Challagundla |
| title |
Range Expansion and the Origin of USA300 North American Epidemic Methicillin-Resistant <italic toggle="yes">Staphylococcus aureus</italic> |
| title_short |
Range Expansion and the Origin of USA300 North American Epidemic Methicillin-Resistant <italic toggle="yes">Staphylococcus aureus</italic> |
| title_full |
Range Expansion and the Origin of USA300 North American Epidemic Methicillin-Resistant <italic toggle="yes">Staphylococcus aureus</italic> |
| title_fullStr |
Range Expansion and the Origin of USA300 North American Epidemic Methicillin-Resistant <italic toggle="yes">Staphylococcus aureus</italic> |
| title_full_unstemmed |
Range Expansion and the Origin of USA300 North American Epidemic Methicillin-Resistant <italic toggle="yes">Staphylococcus aureus</italic> |
| title_sort |
range expansion and the origin of usa300 north american epidemic methicillin-resistant <italic toggle="yes">staphylococcus aureus</italic> |
| publisher |
American Society for Microbiology |
| publishDate |
2018 |
| url |
https://doaj.org/article/7f218b46d58048afa74e73d06b978a9f |
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