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Genomic Characterization and Antimicrobial Susceptibility of Dromedary-Associated Staphylococcaceae from the Horn of Africa

Members of the Staphylococcaceae family, particularly those of the genus Staphylococcus, encompass important human and animal pathogens. We collected and characterized Staphylococcaceae strains from apparently healthy and diseased camels (n = 84) and cattle (n = 7) in Somalia and Kenya. We phenotypi...

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Autores principales: Akarsu, Hatice, Liljander, Anne, Younan, Mario, Brodard, Isabelle, Overesch, Gudrun, Glücks, Ilona, Labroussaa, Fabien, Kuhnert, Peter, Perreten, Vincent, Monecke, Stefan, Drexler, Jan Felix, Corman, Victor Max, Falquet, Laurent, Jores, Joerg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9642023/
https://www.ncbi.nlm.nih.gov/pubmed/36226992
http://dx.doi.org/10.1128/aem.01146-22
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author Akarsu, Hatice
Liljander, Anne
Younan, Mario
Brodard, Isabelle
Overesch, Gudrun
Glücks, Ilona
Labroussaa, Fabien
Kuhnert, Peter
Perreten, Vincent
Monecke, Stefan
Drexler, Jan Felix
Corman, Victor Max
Falquet, Laurent
Jores, Joerg
author_facet Akarsu, Hatice
Liljander, Anne
Younan, Mario
Brodard, Isabelle
Overesch, Gudrun
Glücks, Ilona
Labroussaa, Fabien
Kuhnert, Peter
Perreten, Vincent
Monecke, Stefan
Drexler, Jan Felix
Corman, Victor Max
Falquet, Laurent
Jores, Joerg
author_sort Akarsu, Hatice
collection PubMed
description Members of the Staphylococcaceae family, particularly those of the genus Staphylococcus, encompass important human and animal pathogens. We collected and characterized Staphylococcaceae strains from apparently healthy and diseased camels (n = 84) and cattle (n = 7) in Somalia and Kenya. We phenotypically characterized the strains, including their antimicrobial inhibitory concentrations. Then, we sequenced their genomes using long-read sequencing, closed their genomes, and subsequently compared and mapped their virulence- and resistance-associated gene pools. Genome-based phylogenetics revealed 13 known Staphylococcaceae and at least two novel species. East African strains of different species encompassed novel sequence types and phylogenetically distant clades. About one-third of the strains had non-wild-type MICs. They were resistant to at least one of the following antimicrobials: tetracycline, benzylpenicillin, oxacillin, erythromycin, clindamycin, trimethoprim, gentamicin, or streptomycin, encoded by tet(K), blaZ/bla(ARL), mecA/mecA1, msrA/mphC, salA, dfrG, aacA-aphD, and str, respectively. We identified the first methicillin- and multidrug-resistant camel S. epidermidis strain of sequence type (ST) 1136 in East Africa. The pool of virulence-encoding genes was largest in the S. aureus strains, as expected, although other rather commensal strains contained distinct virulence-encoding genes. We identified toxin-antitoxin (TA) systems such as the hicA/hicB and abiEii/abiEi families, reported here for the first time for certain species of Staphylococcaceae. All strains contained at least one intact prophage sequence, mainly belonging to the Siphoviridae family. We pinpointed potential horizontal gene transfers between camel and cattle strains and also across distinct Staphylococcaceae clades and species. IMPORTANCE Camels are a high value and crucial livestock species in arid and semiarid regions of Africa and gain importance giving the impact of climate change on traditional livestock species. Our current knowledge with respect to Staphylococcaceae infecting camels is very limited compared to that for other livestock species. Better knowledge will foster the development of specific diagnostic assays, guide promising antimicrobial treatment options, and inform about potential zoonotic risks. We characterized 84 Staphylococcaceae strains isolated from camels with respect to their antimicrobial resistance and virulence traits. We detected potentially novel Staphylococcus species, resistances to different classes of antimicrobials, and the first camel multidrug-resistant S. epidermidis strain of sequence type 1136.
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spelling pubmed-96420232022-11-15 Genomic Characterization and Antimicrobial Susceptibility of Dromedary-Associated Staphylococcaceae from the Horn of Africa Akarsu, Hatice Liljander, Anne Younan, Mario Brodard, Isabelle Overesch, Gudrun Glücks, Ilona Labroussaa, Fabien Kuhnert, Peter Perreten, Vincent Monecke, Stefan Drexler, Jan Felix Corman, Victor Max Falquet, Laurent Jores, Joerg Appl Environ Microbiol Evolutionary and Genomic Microbiology Members of the Staphylococcaceae family, particularly those of the genus Staphylococcus, encompass important human and animal pathogens. We collected and characterized Staphylococcaceae strains from apparently healthy and diseased camels (n = 84) and cattle (n = 7) in Somalia and Kenya. We phenotypically characterized the strains, including their antimicrobial inhibitory concentrations. Then, we sequenced their genomes using long-read sequencing, closed their genomes, and subsequently compared and mapped their virulence- and resistance-associated gene pools. Genome-based phylogenetics revealed 13 known Staphylococcaceae and at least two novel species. East African strains of different species encompassed novel sequence types and phylogenetically distant clades. About one-third of the strains had non-wild-type MICs. They were resistant to at least one of the following antimicrobials: tetracycline, benzylpenicillin, oxacillin, erythromycin, clindamycin, trimethoprim, gentamicin, or streptomycin, encoded by tet(K), blaZ/bla(ARL), mecA/mecA1, msrA/mphC, salA, dfrG, aacA-aphD, and str, respectively. We identified the first methicillin- and multidrug-resistant camel S. epidermidis strain of sequence type (ST) 1136 in East Africa. The pool of virulence-encoding genes was largest in the S. aureus strains, as expected, although other rather commensal strains contained distinct virulence-encoding genes. We identified toxin-antitoxin (TA) systems such as the hicA/hicB and abiEii/abiEi families, reported here for the first time for certain species of Staphylococcaceae. All strains contained at least one intact prophage sequence, mainly belonging to the Siphoviridae family. We pinpointed potential horizontal gene transfers between camel and cattle strains and also across distinct Staphylococcaceae clades and species. IMPORTANCE Camels are a high value and crucial livestock species in arid and semiarid regions of Africa and gain importance giving the impact of climate change on traditional livestock species. Our current knowledge with respect to Staphylococcaceae infecting camels is very limited compared to that for other livestock species. Better knowledge will foster the development of specific diagnostic assays, guide promising antimicrobial treatment options, and inform about potential zoonotic risks. We characterized 84 Staphylococcaceae strains isolated from camels with respect to their antimicrobial resistance and virulence traits. We detected potentially novel Staphylococcus species, resistances to different classes of antimicrobials, and the first camel multidrug-resistant S. epidermidis strain of sequence type 1136. American Society for Microbiology 2022-10-13 /pmc/articles/PMC9642023/ /pubmed/36226992 http://dx.doi.org/10.1128/aem.01146-22 Text en Copyright © 2022 Akarsu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Evolutionary and Genomic Microbiology
Akarsu, Hatice
Liljander, Anne
Younan, Mario
Brodard, Isabelle
Overesch, Gudrun
Glücks, Ilona
Labroussaa, Fabien
Kuhnert, Peter
Perreten, Vincent
Monecke, Stefan
Drexler, Jan Felix
Corman, Victor Max
Falquet, Laurent
Jores, Joerg
Genomic Characterization and Antimicrobial Susceptibility of Dromedary-Associated Staphylococcaceae from the Horn of Africa
title Genomic Characterization and Antimicrobial Susceptibility of Dromedary-Associated Staphylococcaceae from the Horn of Africa
title_full Genomic Characterization and Antimicrobial Susceptibility of Dromedary-Associated Staphylococcaceae from the Horn of Africa
title_fullStr Genomic Characterization and Antimicrobial Susceptibility of Dromedary-Associated Staphylococcaceae from the Horn of Africa
title_full_unstemmed Genomic Characterization and Antimicrobial Susceptibility of Dromedary-Associated Staphylococcaceae from the Horn of Africa
title_short Genomic Characterization and Antimicrobial Susceptibility of Dromedary-Associated Staphylococcaceae from the Horn of Africa
title_sort genomic characterization and antimicrobial susceptibility of dromedary-associated staphylococcaceae from the horn of africa
topic Evolutionary and Genomic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9642023/
https://www.ncbi.nlm.nih.gov/pubmed/36226992
http://dx.doi.org/10.1128/aem.01146-22
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