Staphylococcus epidermidis Phages Transduce Antimicrobial
Resistance Plasmids and Mobilize Chromosomal Islands

J 2021

Staphylococcus epidermidis Phages Transduce Antimicrobial Resistance Plasmids and Mobilize Chromosomal Islands

FIŠAROVÁ, Lenka, Tibor BOTKA, Xin DU, Ivana MAŠLAŇOVÁ, Pavol BÁRDY et. al.

Basic information

Original name

Staphylococcus epidermidis Phages Transduce Antimicrobial Resistance Plasmids and Mobilize Chromosomal Islands

Authors

FIŠAROVÁ, Lenka (203 Czech Republic, belonging to the institution), Tibor BOTKA (203 Czech Republic, belonging to the institution), Xin DU (156 China), Ivana MAŠLAŇOVÁ (203 Czech Republic, belonging to the institution), Pavol BÁRDY (703 Slovakia, belonging to the institution), Roman PANTŮČEK (203 Czech Republic, belonging to the institution), Martin BENEŠÍK (203 Czech Republic, belonging to the institution), Pavel ROUDNICKÝ (203 Czech Republic, belonging to the institution), Volker WINSTEL (276 Germany), Jesper LARSEN (208 Denmark), Ralf ROSENSTEIN (276 Germany), Andreas PESCHEL (276 Germany) and Jiří DOŠKAŘ (203 Czech Republic, guarantor, belonging to the institution)

Edition

mSphere, Washington, DC, USA, American Society for Microbiology, 2021, 2379-5042

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10608 Biochemistry and molecular biology

Country of publisher

United States of America

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 5.029

RIV identification code

RIV/00216224:14310/21:00118971

Organization unit

Faculty of Science

DOI

http://dx.doi.org/10.1128/mSphere.00223-21

UT WoS

000663083400008

Keywords in English

bacteriophages; Staphylococcus epidermidis; antibiotic resistance; horizontal gene transfer; pathogenicity islands; transduction

Abstract

V originále

Staphylococcus epidermidis is a leading opportunistic pathogen causing nosocomial infections that is notable for its ability to form a biofilm and for its high rates of antibiotic resistance. It serves as a reservoir of multiple antimicrobial resistance genes that spread among the staphylococcal population by horizontal gene transfer such as transduction. While phage-mediated transduction is well studied in Staphylococcus aureus, S. epidermidis transducing phages have not been described in detail yet. Here, we report the characteristics of four phages, 27, 48, 456, and 459, previously used for S. epidermidis phage typing, and the newly isolated phage E72, from a clinical S. epidermidis strain. The phages, classified in the family Siphoviridae and genus Phietavirus, exhibited an S. epidermidis-specific host range, and together they infected 49% of the 35 strains tested. A whole-genome comparison revealed evolutionary relatedness to transducing S. aureus phietaviruses. In accordance with this, all the tested phages were capable of transduction with high frequencies up to 10−4 among S. epidermidis strains from different clonal complexes. Plasmids with sizes from 4 to 19 kb encoding resistance to streptomycin, tetracycline, and chloramphenicol were transferred. We provide here the first evidence of a phage-inducible chromosomal island transfer in S. epidermidis. Similarly to S. aureus pathogenicity islands, the transfer was accompanied by phage capsid remodeling; however, the interfering protein encoded by the island was distinct. Our findings underline the role of S. epidermidis temperate phages in the evolution of S. epidermidis strains by horizontal gene transfer, which can also be utilized for S. epidermidis genetic studies.

Links

GA18-13064S, research and development project

Name: Analýza interakcí mezi polyvalentním terapeutickým fágem druhu Twort-like a jeho hostitelem Staphylococcus aureus

Investor: Czech Science Foundation

LQ1601, research and development project

Name: CEITEC 2020 (Acronym: CEITEC2020)

Investor: Ministry of Education, Youth and Sports of the CR

MUNI/A/1522/2020, interní kód MU

Name: Podpora výzkumné činnosti studentů molekulární biologie a genetiky 9 (Acronym: MBG9)

Investor: Masaryk University

90127, large research infrastructures

Name: CIISB II

90132, large research infrastructures

Name: NCMG II

Files attached

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Request the author's version of the file

Citovat

FIŠAROVÁ, Lenka, Tibor BOTKA, Xin DU, Ivana MAŠLAŇOVÁ, Pavol BÁRDY, Roman PANTŮČEK, Martin BENEŠÍK, Pavel ROUDNICKÝ, Volker WINSTEL, Jesper LARSEN, Ralf ROSENSTEIN, Andreas PESCHEL and Jiří DOŠKAŘ. Staphylococcus epidermidis Phages Transduce Antimicrobial Resistance Plasmids and Mobilize Chromosomal Islands. mSphere. Washington, DC, USA: American Society for Microbiology, 2021, vol. 6, No 3, p. 1-19. ISSN 2379-5042. Available from: https://dx.doi.org/10.1128/mSphere.00223-21.

@article{1769437,
   author = {Fišarová, Lenka and Botka, Tibor and Du, Xin and Mašlaňová, Ivana and Bárdy, Pavol and Pantůček, Roman and Benešík, Martin and Roudnický, Pavel and Winstel, Volker and Larsen, Jesper and Rosenstein, Ralf and Peschel, Andreas and Doškař, Jiří},
   article_location = {Washington, DC, USA},
   article_number = {3},
   doi = {http://dx.doi.org/10.1128/mSphere.00223-21},
   keywords = {bacteriophages; Staphylococcus epidermidis; antibiotic resistance; horizontal gene transfer; pathogenicity islands; transduction},
   language = {eng},
   issn = {2379-5042},
   journal = {mSphere},
   title = {Staphylococcus epidermidis Phages Transduce Antimicrobial Resistance Plasmids and Mobilize Chromosomal Islands},
   url = {https://journals.asm.org/doi/10.1128/mSphere.00223-21},
   volume = {6},
   year = {2021}
}

TY  - JOUR
ID  - 1769437
AU  - Fišarová, Lenka - Botka, Tibor - Du, Xin - Mašlaňová, Ivana - Bárdy, Pavol - Pantůček, Roman - Benešík, Martin - Roudnický, Pavel - Winstel, Volker - Larsen, Jesper - Rosenstein, Ralf - Peschel, Andreas - Doškař, Jiří
PY  - 2021
TI  - Staphylococcus epidermidis Phages Transduce Antimicrobial Resistance Plasmids and Mobilize Chromosomal Islands
JF  - mSphere
VL  - 6
IS  - 3
SP  - 1-19
EP  - 1-19
PB  - American Society for Microbiology
SN  - 23795042
KW  - bacteriophages
KW  - Staphylococcus epidermidis
KW  - antibiotic resistance
KW  - horizontal gene transfer
KW  - pathogenicity islands
KW  - transduction
UR  - https://journals.asm.org/doi/10.1128/mSphere.00223-21
N2  - Staphylococcus epidermidis is a leading opportunistic pathogen causing nosocomial infections that is notable for its ability to form a biofilm and for its high rates of antibiotic resistance. It serves as a reservoir of multiple antimicrobial resistance genes that spread among the staphylococcal population by horizontal gene transfer such as transduction. While phage-mediated transduction is well studied in Staphylococcus aureus, S. epidermidis transducing phages have not been described in detail yet. Here, we report the characteristics of four phages, 27, 48, 456, and 459, previously used for S. epidermidis phage typing, and the newly isolated phage E72, from a clinical S. epidermidis strain. The phages, classified in the family Siphoviridae and genus Phietavirus, exhibited an S. epidermidis-specific host range, and together they infected 49% of the 35 strains tested. A whole-genome comparison revealed evolutionary relatedness to transducing S. aureus phietaviruses. In accordance with this, all the tested phages were capable of transduction with high frequencies up to 10−4 among S. epidermidis strains from different clonal complexes. Plasmids with sizes from 4 to 19 kb encoding resistance to streptomycin, tetracycline, and chloramphenicol were transferred. We provide here the first evidence of a phage-inducible chromosomal island transfer in S. epidermidis. Similarly to S. aureus pathogenicity islands, the transfer was accompanied by phage capsid remodeling; however, the interfering protein encoded by the island was distinct. Our findings underline the role of S. epidermidis temperate phages in the evolution of S. epidermidis strains by horizontal gene transfer, which can also be utilized for S. epidermidis genetic studies.
ER  -

FIŠAROVÁ, Lenka, Tibor BOTKA, Xin DU, Ivana MAŠLAŇOVÁ, Pavol BÁRDY, Roman PANTŮČEK, Martin BENEŠÍK, Pavel ROUDNICKÝ, Volker WINSTEL, Jesper LARSEN, Ralf ROSENSTEIN, Andreas PESCHEL and Jiří DOŠKAŘ. Staphylococcus epidermidis Phages Transduce Antimicrobial Resistance Plasmids and Mobilize Chromosomal Islands. \textit{mSphere}. Washington, DC, USA: American Society for Microbiology, 2021, vol.~6, No~3, p.~1-19. ISSN~2379-5042. Available from: https://dx.doi.org/10.1128/mSphere.00223-21.

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