The Resistome and Mobilome of Multidrug-Resistant Staphylococcus sciuri C2865 Unveil a Transferable Trimethoprim Resistance Gene, Designated dfrE, Spread Unnoticed


Por: Gomez-Sanz, E, Haro-Moreno, J, Jensen, S, Roda-Garcia, J and Lopez-Perez, M

Publicada: 1 ago 2021
Resumen:
Methicillin-resistant Staphylococcus sciuri (MRSS) strain C2865 from a stranded dog in Nigeria was trimethoprim (TMP) resistant but lacked formerly described staphylococcal TMP-resistant dihydrofolate reductase genes (dfr). Whole-genome sequencing, comparative genomics, and pan-genome analyses were pur-sued to unveil the molecular bases for TMP resistance via resistome and mobilome profiling. MRSS C2865 comprised a species subcluster and positioned just above the intraspecies boundary. Lack of species host tropism was observed. S. sciuri exhibited an open pan-genome, while MRSS C2865 harbored the highest number of unique genes (75% associated with mobilome). Within this fraction, we discovered a trans-ferable TMP resistance gene, named dfrE, which confers high-level TMP resistance in Staphylococcus aureus and Escherichia coli. dfrE was located in a novel multidrug re-sistance mosaic plasmid (pUR2865-34) encompassing adaptive, mobilization, and segregational stability traits. dfrE was formerly denoted as dfr_like in Exiguobacterium spp. from fish farm sediment in China but escaped identification in one macrococcal and diverse staphylococcal genomes in different Asian countries. dfrE shares the highest identity with dfr of soil-related Paenibacillus anaericanus (68%). Data analysis discloses that dfrE has emerged from a single ancestor and places S. sciuri as a plau-sible donor. C2865 unique fraction additionally enclosed novel chromosomal mobile islands, including a multidrug-resistant pseudo-SCCmec cassette, three apparently functional prophages (Siphoviridae), and an SaPI4-related staphylococcal pathogenic-ity island. Since dfrE seems not yet common in staphylococcal clinical specimens, our data promote early surveillance and enable molecular diagnosis. We evidence the genome plasticity of S. sciuri and highlight its role as a resourceful reservoir for adaptive traits. IMPORTANCE The discovery and surveillance of antimicrobial resistance genes (AMRG) and their mobilization platforms are critical to understand the evolution of bacterial re-sistance and to restrain further expansion. Limited genomic data are available on Staphylococcus sciuri; regardless, it is considered a reservoir for critical AMRG and mo-bile elements. We uncover a transferable staphylococcal TMP resistance gene, named dfrE, in a novel mosaic plasmid harboring additional resistance, adaptive, and self-stabi-lization features. dfrE is present but evaded detection in diverse species from varied sources geographically distant. Our analyses evidence that the dfrE-carrying element has emerged from a single ancestor and position S. sciuri as the donor species for dfrE spread. We also identify novel mobilizable chromosomal islands encompassing AMRG and three unrelated prophages. We prove high intraspecies heterogenicity and genome plasticity for S. sciuri. This work highlights the importance of genome-wide ecological studies to facilitate identification, characterization, and evolution routes of bacteria adaptive features.

Filiaciones:
Gomez-Sanz, E:
 ETHZ, Inst Food Nutr & Hlth, Zurich, Switzerland

 Ctr Invest Biomed La Rioja CIBIR, Area Microbiol Mol, Logrono, Spain

:
 Univ Miguel Hernandez, Div Microbiol, Evolutionary Genom Grp, Alicante, Spain

Jensen, S:
 Western Sydney Univ, Sch Med, Infect Dis & Microbiol, Sydney, NSW, Australia

 Ingham Inst Appl Med Res, Antimicrobial Resistance & Mobile Elements Grp, Sydney, NSW, Australia

Roda-Garcia, J:
 Univ Miguel Hernandez, Div Microbiol, Evolutionary Genom Grp, Alicante, Spain

:
 Univ Miguel Hernandez, Div Microbiol, Evolutionary Genom Grp, Alicante, Spain
ISSN: 23795077





mSystems
Editorial
American Society for Microbiology, 1752 N ST NW, WASHINGTON, DC 20036-2904 USA, Estados Unidos America
Tipo de documento: Article
Volumen: 6 Número: 4
Páginas:
WOS Id: 000709862800001
ID de PubMed: 34374564
imagen gold, Green Published, Green Accepted

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