TY - JOUR
T1 - Phylogenomic classification and the evolution of Clonal complex 5 methicillin-resistant Staphylococcus aureus in the Western Hemisphere
AU - Challagundla, Lavanya
AU - Reyes, Jinnethe
AU - Rafiqullah, Iftekhar
AU - Sordelli, Daniel O.
AU - Echaniz-Aviles, Gabriela
AU - Velazquez-Meza, Maria E.
AU - Castillo-Ramírez, Santiago
AU - Fittipaldi, Nahuel
AU - Feldgarden, Michael
AU - Chapman, Sinéad B.
AU - Calderwood, Michael S.
AU - Carvajal, Lina P.
AU - Rincon, Sandra
AU - Hanson, Blake
AU - Planet, Paul J.
AU - Arias, Cesar A.
AU - Diaz, Lorena
AU - Robinson, D. Ashley
N1 - Funding Information:
For provision of bacterial isolates, we gratefully acknowledge Rayo Morfin-Otero and Eduardo Rodriguez-Noriega from the Antiguo Hospital Civil "Fray Antonio Alcalde," Guadalajara, Jalisco, Mexico; Elvira Garza-González from the Hospital Universitario "Dr. Jose Eleuterio Gonzalez," Monterrey, Nuevo Leon, Mexico; Patricia Cornejo-Juárez and Patricia Volkow-Fernández, from the Instituto Nacional de Cancerologia, Mexico City, Mexico; The Canadian Nosocomial Infection Surveillance Program. For assistance with genome sequencing, we gratefully acknowledge Xiao Luo from UMMC; An Dinh from the University of Texas Health Science Center.This work was supported in part by NIH grant R01-GM080602 to DR. The work of JR and LD, respectively, was supported by grants COL130871250417 and COL130874455850 from Colciencias. The work of DS was funded by grants ANPCyT PICT 2010-00941 and UBACyT 20020130100331BA. The work of MF was supported by the intramural research program of the National Library of Medicine, National Institutes of Health. CA was supported by NIH-NIAID award K24 AI121296. This project was funded in part with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under Contract No.: HHSN272200900018C. The work performed through the UMMC's Molecular and Genomics Facility was supported in part by funds from the NIGMS, including Mississippi INBRE (P20GM103476), Center for Psychiatric Neuroscience (CPN)-COBRE (P30GM103328), Obesity, Cardiorenal and Metabolic Diseases-COBRE (P20GM104357), and Mississippi Center of Excellence in Perinatal Research (MS-CEPR)-COBRE (P20GM121334). The content of the manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Publisher Copyright:
© 2018 Challagundla, Reyes, Rafiqullah, Sordelli, Echaniz-Aviles, Velazquez-Meza, Castillo-Ramírez, Fittipaldi, Feldgarden, Chapman, Calderwood, Carvajal, Rincon, Hanson, Planet, Arias, Diaz and Robinson.
PY - 2018/8/22
Y1 - 2018/8/22
N2 - Clonal complex 5 methicillin-resistant Staphylococcus aureus (CC5-MRSA) includes multiple prevalent clones that cause hospital-associated infections in the Western Hemisphere. Here, we present a phylogenomic study of these MRSA to reveal their phylogeny, spatial and temporal population structure, and the evolution of selected traits. We studied 598 genome sequences, including 409 newly generated sequences, from 11 countries in Central, North, and South America, and references from Asia and Europe. An early-branching CC5-Basal clade is well-dispersed geographically, is methicillin-susceptible and MRSA predominantly of ST5-IV such as the USA800 clone, and includes separate subclades for avian and porcine strains. In the early 1970s and early 1960s, respectively, two clades appeared that subsequently underwent major expansions in the Western Hemisphere: a CC5-I clade in South America and a CC5-II clade largely in Central and North America. The CC5-I clade includes the ST5-I Chilean/Cordobes clone, and the ST228-I South German clone as an early offshoot, but is distinct from other ST5-I clones from Europe that nest within CC5-Basal. The CC5-II clade includes divergent strains of the ST5-II USA100 clone, various other clones, and most known vancomycin-resistant strains of S. aureus, but is distinct from ST5-II strain N315 from Japan that nests within CC5-Basal. The recombination rate of CC5 was much lower than has been reported for other S. aureus genetic backgrounds, which indicates that recurrence of vancomycin resistance in CC5 is not likely due to an enhanced promiscuity. An increased number of antibiotic resistances and decreased number of toxins with distance from the CC5 tree root were observed. Of note, the expansions of the CC5-I and CC5-II clades in the Western Hemisphere were preceded by convergent gains of resistance to fluoroquinolone, macrolide, and lincosamide antibiotics, and convergent losses of the staphylococcal enterotoxin p (sep) gene from the immune evasion gene cluster of phage ΦSa3. Unique losses of surface proteins were also noted for these two clades. In summary, our study has determined the relationships of different clades and clones of CC5 and has revealed genomic changes for increased antibiotic resistance and decreased virulence associated with the expansions of these MRSA in the Western Hemisphere.
AB - Clonal complex 5 methicillin-resistant Staphylococcus aureus (CC5-MRSA) includes multiple prevalent clones that cause hospital-associated infections in the Western Hemisphere. Here, we present a phylogenomic study of these MRSA to reveal their phylogeny, spatial and temporal population structure, and the evolution of selected traits. We studied 598 genome sequences, including 409 newly generated sequences, from 11 countries in Central, North, and South America, and references from Asia and Europe. An early-branching CC5-Basal clade is well-dispersed geographically, is methicillin-susceptible and MRSA predominantly of ST5-IV such as the USA800 clone, and includes separate subclades for avian and porcine strains. In the early 1970s and early 1960s, respectively, two clades appeared that subsequently underwent major expansions in the Western Hemisphere: a CC5-I clade in South America and a CC5-II clade largely in Central and North America. The CC5-I clade includes the ST5-I Chilean/Cordobes clone, and the ST228-I South German clone as an early offshoot, but is distinct from other ST5-I clones from Europe that nest within CC5-Basal. The CC5-II clade includes divergent strains of the ST5-II USA100 clone, various other clones, and most known vancomycin-resistant strains of S. aureus, but is distinct from ST5-II strain N315 from Japan that nests within CC5-Basal. The recombination rate of CC5 was much lower than has been reported for other S. aureus genetic backgrounds, which indicates that recurrence of vancomycin resistance in CC5 is not likely due to an enhanced promiscuity. An increased number of antibiotic resistances and decreased number of toxins with distance from the CC5 tree root were observed. Of note, the expansions of the CC5-I and CC5-II clades in the Western Hemisphere were preceded by convergent gains of resistance to fluoroquinolone, macrolide, and lincosamide antibiotics, and convergent losses of the staphylococcal enterotoxin p (sep) gene from the immune evasion gene cluster of phage ΦSa3. Unique losses of surface proteins were also noted for these two clades. In summary, our study has determined the relationships of different clades and clones of CC5 and has revealed genomic changes for increased antibiotic resistance and decreased virulence associated with the expansions of these MRSA in the Western Hemisphere.
KW - Convergent evolution
KW - Local adaptation
KW - MRSA
KW - Methicillin-resistant Staphylococcus aureus
KW - Phylogenomics
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U2 - 10.3389/fmicb.2018.01901
DO - 10.3389/fmicb.2018.01901
M3 - Article
AN - SCOPUS:85052615715
VL - 9
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
SN - 1664-302X
IS - AUG
M1 - 1901
ER -