Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus

Autores
Challagundla, Lavanya; Luo, Xiao; Tickler, Isabella A.; Didelot, Xavier; Coleman, David C.; Shore, Anna C.; Coombs, Geoffrey W.; Sordelli, Daniel Oscar; Brown, Eric L.; Skov, Robert; Larsen, Anders Rhod; Reyes, Jinnethe; Robledo, Iraida E.; Vazquez, Guillermo Javier; Rivera, Raul; Fey, Paul D.; Stevenson, Kurt; Wang, Shu-Hua; Kreiswirth, Barry N.; Mediavilla, Jose R.; Arias, Cesar A.; Planet, Paul J.; Nolan, Rathel L.; Tenover, Fred C.; Goering, Richard V.; Robinson, D. Ashley
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: Challagundla, Lavanya. University of Mississippi; Estados Unidos
Fil: Luo, Xiao. University of Mississippi; Estados Unidos
Fil: Tickler, Isabella A.. Cepheid; Estados Unidos
Fil: Didelot, Xavier. Imperial College London; Reino Unido
Fil: Coleman, David C.. Universidad de Dublin; Irlanda
Fil: Shore, Anna C.. Universidad de Dublin; Irlanda
Fil: Coombs, Geoffrey W.. PathWest Laboratory Medicine, Fiona Stanley Hospital; Australia
Fil: Sordelli, Daniel Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones en Microbiología y Parasitología Médica. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones en Microbiología y Parasitología Médica; Argentina
Fil: Brown, Eric L.. University of Texas; Estados Unidos
Fil: Skov, Robert. Statens Serum Institut; Dinamarca
Fil: Larsen, Anders Rhod. Statens Serum Institut; Dinamarca
Fil: Reyes, Jinnethe. Universidad El Bosque; Colombia
Fil: Robledo, Iraida E.. Universidad de Puerto Rico; Puerto Rico
Fil: Vazquez, Guillermo Javier. Universidad de Puerto Rico; Puerto Rico
Fil: Rivera, Raul. Universidad de Puerto Rico; Puerto Rico
Fil: Fey, Paul D.. University of Nebraska; Estados Unidos
Fil: Stevenson, Kurt. Ohio State University; Estados Unidos
Fil: Wang, Shu-Hua. Ohio State University; Estados Unidos
Fil: Kreiswirth, Barry N.. Rutgers University. New Jersey Medical School; Estados Unidos
Fil: Mediavilla, Jose R.. Rutgers University. New Jersey Medical School; Estados Unidos
Fil: Arias, Cesar A.. University of Texas; Estados Unidos
Fil: Planet, Paul J.. University of Pennsylvania; Estados Unidos
Fil: Nolan, Rathel L.. University of Mississippi; Estados Unidos
Fil: Tenover, Fred C.. Cepheid; Estados Unidos
Fil: Goering, Richard V.. Creighton University; Estados Unidos
Fil: Robinson, D. Ashley. University of Mississippi; Estados Unidos
Materia
EPIDEMICS
FLUOROQUINOLONES
FOUNDER EFFECTS
GENETIC DRIFT
POPULATION GENETICS
RANGE EXPANSION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/89728

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oai_identifier_str oai:ri.conicet.gov.ar:11336/89728
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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureusChallagundla, LavanyaLuo, XiaoTickler, Isabella A.Didelot, XavierColeman, David C.Shore, Anna C.Coombs, Geoffrey W.Sordelli, Daniel OscarBrown, Eric L.Skov, RobertLarsen, Anders RhodReyes, JinnetheRobledo, Iraida E.Vazquez, Guillermo JavierRivera, RaulFey, Paul D.Stevenson, KurtWang, Shu-HuaKreiswirth, Barry N.Mediavilla, Jose R.Arias, Cesar A.Planet, Paul J.Nolan, Rathel L.Tenover, Fred C.Goering, Richard V.Robinson, D. AshleyEPIDEMICSFLUOROQUINOLONESFOUNDER EFFECTSGENETIC DRIFTPOPULATION GENETICSRANGE EXPANSIONhttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3The 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.Fil: Challagundla, Lavanya. University of Mississippi; Estados UnidosFil: Luo, Xiao. University of Mississippi; Estados UnidosFil: Tickler, Isabella A.. Cepheid; Estados UnidosFil: Didelot, Xavier. Imperial College London; Reino UnidoFil: Coleman, David C.. Universidad de Dublin; IrlandaFil: Shore, Anna C.. Universidad de Dublin; IrlandaFil: Coombs, Geoffrey W.. PathWest Laboratory Medicine, Fiona Stanley Hospital; AustraliaFil: Sordelli, Daniel Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones en Microbiología y Parasitología Médica. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones en Microbiología y Parasitología Médica; ArgentinaFil: Brown, Eric L.. University of Texas; Estados UnidosFil: Skov, Robert. Statens Serum Institut; DinamarcaFil: Larsen, Anders Rhod. Statens Serum Institut; DinamarcaFil: Reyes, Jinnethe. Universidad El Bosque; ColombiaFil: Robledo, Iraida E.. Universidad de Puerto Rico; Puerto RicoFil: Vazquez, Guillermo Javier. Universidad de Puerto Rico; Puerto RicoFil: Rivera, Raul. Universidad de Puerto Rico; Puerto RicoFil: Fey, Paul D.. University of Nebraska; Estados UnidosFil: Stevenson, Kurt. Ohio State University; Estados UnidosFil: Wang, Shu-Hua. Ohio State University; Estados UnidosFil: Kreiswirth, Barry N.. Rutgers University. New Jersey Medical School; Estados UnidosFil: Mediavilla, Jose R.. Rutgers University. New Jersey Medical School; Estados UnidosFil: Arias, Cesar A.. University of Texas; Estados UnidosFil: Planet, Paul J.. University of Pennsylvania; Estados UnidosFil: Nolan, Rathel L.. University of Mississippi; Estados UnidosFil: Tenover, Fred C.. Cepheid; Estados UnidosFil: Goering, Richard V.. Creighton University; Estados UnidosFil: Robinson, D. Ashley. University of Mississippi; Estados UnidosAmerican Society for Microbiology2018-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/89728Challagundla, Lavanya; Luo, Xiao; Tickler, Isabella A.; Didelot, Xavier; Coleman, David C.; et al.; Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus; American Society for Microbiology; mBio; 9; 1; 1-2018; 1-15; e02016-172150-7511CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://mbio.asm.org/content/9/1/e02016-17info:eu-repo/semantics/altIdentifier/doi/10.1128/mBio.02016-17info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:52:31Zoai:ri.conicet.gov.ar:11336/89728instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:52:31.887CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus
title Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus
spellingShingle Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus
Challagundla, Lavanya
EPIDEMICS
FLUOROQUINOLONES
FOUNDER EFFECTS
GENETIC DRIFT
POPULATION GENETICS
RANGE EXPANSION
title_short Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus
title_full Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus
title_fullStr Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus
title_full_unstemmed Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus
title_sort Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus
dc.creator.none.fl_str_mv Challagundla, Lavanya
Luo, Xiao
Tickler, Isabella A.
Didelot, Xavier
Coleman, David C.
Shore, Anna C.
Coombs, Geoffrey W.
Sordelli, Daniel Oscar
Brown, Eric L.
Skov, Robert
Larsen, Anders Rhod
Reyes, Jinnethe
Robledo, Iraida E.
Vazquez, Guillermo Javier
Rivera, Raul
Fey, Paul D.
Stevenson, Kurt
Wang, Shu-Hua
Kreiswirth, Barry N.
Mediavilla, Jose R.
Arias, Cesar A.
Planet, Paul J.
Nolan, Rathel L.
Tenover, Fred C.
Goering, Richard V.
Robinson, D. Ashley
author Challagundla, Lavanya
author_facet Challagundla, Lavanya
Luo, Xiao
Tickler, Isabella A.
Didelot, Xavier
Coleman, David C.
Shore, Anna C.
Coombs, Geoffrey W.
Sordelli, Daniel Oscar
Brown, Eric L.
Skov, Robert
Larsen, Anders Rhod
Reyes, Jinnethe
Robledo, Iraida E.
Vazquez, Guillermo Javier
Rivera, Raul
Fey, Paul D.
Stevenson, Kurt
Wang, Shu-Hua
Kreiswirth, Barry N.
Mediavilla, Jose R.
Arias, Cesar A.
Planet, Paul J.
Nolan, Rathel L.
Tenover, Fred C.
Goering, Richard V.
Robinson, D. Ashley
author_role author
author2 Luo, Xiao
Tickler, Isabella A.
Didelot, Xavier
Coleman, David C.
Shore, Anna C.
Coombs, Geoffrey W.
Sordelli, Daniel Oscar
Brown, Eric L.
Skov, Robert
Larsen, Anders Rhod
Reyes, Jinnethe
Robledo, Iraida E.
Vazquez, Guillermo Javier
Rivera, Raul
Fey, Paul D.
Stevenson, Kurt
Wang, Shu-Hua
Kreiswirth, Barry N.
Mediavilla, Jose R.
Arias, Cesar A.
Planet, Paul J.
Nolan, Rathel L.
Tenover, Fred C.
Goering, Richard V.
Robinson, D. Ashley
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv EPIDEMICS
FLUOROQUINOLONES
FOUNDER EFFECTS
GENETIC DRIFT
POPULATION GENETICS
RANGE EXPANSION
topic EPIDEMICS
FLUOROQUINOLONES
FOUNDER EFFECTS
GENETIC DRIFT
POPULATION GENETICS
RANGE EXPANSION
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv 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.
Fil: Challagundla, Lavanya. University of Mississippi; Estados Unidos
Fil: Luo, Xiao. University of Mississippi; Estados Unidos
Fil: Tickler, Isabella A.. Cepheid; Estados Unidos
Fil: Didelot, Xavier. Imperial College London; Reino Unido
Fil: Coleman, David C.. Universidad de Dublin; Irlanda
Fil: Shore, Anna C.. Universidad de Dublin; Irlanda
Fil: Coombs, Geoffrey W.. PathWest Laboratory Medicine, Fiona Stanley Hospital; Australia
Fil: Sordelli, Daniel Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones en Microbiología y Parasitología Médica. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones en Microbiología y Parasitología Médica; Argentina
Fil: Brown, Eric L.. University of Texas; Estados Unidos
Fil: Skov, Robert. Statens Serum Institut; Dinamarca
Fil: Larsen, Anders Rhod. Statens Serum Institut; Dinamarca
Fil: Reyes, Jinnethe. Universidad El Bosque; Colombia
Fil: Robledo, Iraida E.. Universidad de Puerto Rico; Puerto Rico
Fil: Vazquez, Guillermo Javier. Universidad de Puerto Rico; Puerto Rico
Fil: Rivera, Raul. Universidad de Puerto Rico; Puerto Rico
Fil: Fey, Paul D.. University of Nebraska; Estados Unidos
Fil: Stevenson, Kurt. Ohio State University; Estados Unidos
Fil: Wang, Shu-Hua. Ohio State University; Estados Unidos
Fil: Kreiswirth, Barry N.. Rutgers University. New Jersey Medical School; Estados Unidos
Fil: Mediavilla, Jose R.. Rutgers University. New Jersey Medical School; Estados Unidos
Fil: Arias, Cesar A.. University of Texas; Estados Unidos
Fil: Planet, Paul J.. University of Pennsylvania; Estados Unidos
Fil: Nolan, Rathel L.. University of Mississippi; Estados Unidos
Fil: Tenover, Fred C.. Cepheid; Estados Unidos
Fil: Goering, Richard V.. Creighton University; Estados Unidos
Fil: Robinson, D. Ashley. University of Mississippi; Estados Unidos
description 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.
publishDate 2018
dc.date.none.fl_str_mv 2018-01
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/89728
Challagundla, Lavanya; Luo, Xiao; Tickler, Isabella A.; Didelot, Xavier; Coleman, David C.; et al.; Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus; American Society for Microbiology; mBio; 9; 1; 1-2018; 1-15; e02016-17
2150-7511
CONICET Digital
CONICET
url http://hdl.handle.net/11336/89728
identifier_str_mv Challagundla, Lavanya; Luo, Xiao; Tickler, Isabella A.; Didelot, Xavier; Coleman, David C.; et al.; Range expansion and the origin of USA300 north american epidemic methicillin-resistant Staphylococcus aureus; American Society for Microbiology; mBio; 9; 1; 1-2018; 1-15; e02016-17
2150-7511
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://mbio.asm.org/content/9/1/e02016-17
info:eu-repo/semantics/altIdentifier/doi/10.1128/mBio.02016-17
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
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application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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