Novel Bacteriophage Specific against Staphylococcus epidermidis and with Antibiofilm Activity

has emerged as the most important pathogen in infections related to indwelling medical devices, and although these infections are not life-threatening, their frequency and the fact that they are extremely difficult to treat represent a serious burden on the public health system. Treatment is complic...

Full description

Saved in:
Bibliographic Details
Published inViruses Vol. 14; no. 6; p. 1340
Main Authors Fanaei Pirlar, Rima, Wagemans, Jeroen, Ponce Benavente, Luis, Lavigne, Rob, Trampuz, Andrej, Gonzalez Moreno, Mercedes
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 20.06.2022
MDPI
Subjects
Online AccessGet full text

Cover

Loading…
Abstract has emerged as the most important pathogen in infections related to indwelling medical devices, and although these infections are not life-threatening, their frequency and the fact that they are extremely difficult to treat represent a serious burden on the public health system. Treatment is complicated by specific antibiotic resistance genes and the formation of biofilms. Hence, novel therapeutic strategies are needed to fight these infections. A novel bacteriophage CUB-EPI_14 specific to the bacterial species was isolated from sewage and characterized genomically and phenotypically. Its genome contains a total of 46,098 bp and 63 predicted genes, among which some have been associated with packaging and lysis-associated proteins, structural proteins, or DNA- and metabolism-associated proteins. No lysogeny-associated proteins or known virulence proteins were identified in the phage genome. CUB-EPI_14 showed stability over a wide range of temperatures (from -20 °C to 50 °C) and pH values (pH 3-pH 12) and a narrow host range against . Potent antimicrobial and antibiofilm activities were observed when the phage was tested against a highly susceptible bacterial isolate. These encouraging results open the door to new therapeutic opportunities in the fight against resilient biofilm-associated infections caused by .
AbstractList Staphylococcus epidermidis has emerged as the most important pathogen in infections related to indwelling medical devices, and although these infections are not life-threatening, their frequency and the fact that they are extremely difficult to treat represent a serious burden on the public health system. Treatment is complicated by specific antibiotic resistance genes and the formation of biofilms. Hence, novel therapeutic strategies are needed to fight these infections. A novel bacteriophage CUB-EPI_14 specific to the bacterial species S. epidermidis was isolated from sewage and characterized genomically and phenotypically. Its genome contains a total of 46,098 bp and 63 predicted genes, among which some have been associated with packaging and lysis-associated proteins, structural proteins, or DNA- and metabolism-associated proteins. No lysogeny-associated proteins or known virulence proteins were identified in the phage genome. CUB-EPI_14 showed stability over a wide range of temperatures (from −20 °C to 50 °C) and pH values (pH 3–pH 12) and a narrow host range against S. epidermidis . Potent antimicrobial and antibiofilm activities were observed when the phage was tested against a highly susceptible bacterial isolate. These encouraging results open the door to new therapeutic opportunities in the fight against resilient biofilm-associated infections caused by S. epidermidis .
has emerged as the most important pathogen in infections related to indwelling medical devices, and although these infections are not life-threatening, their frequency and the fact that they are extremely difficult to treat represent a serious burden on the public health system. Treatment is complicated by specific antibiotic resistance genes and the formation of biofilms. Hence, novel therapeutic strategies are needed to fight these infections. A novel bacteriophage CUB-EPI_14 specific to the bacterial species was isolated from sewage and characterized genomically and phenotypically. Its genome contains a total of 46,098 bp and 63 predicted genes, among which some have been associated with packaging and lysis-associated proteins, structural proteins, or DNA- and metabolism-associated proteins. No lysogeny-associated proteins or known virulence proteins were identified in the phage genome. CUB-EPI_14 showed stability over a wide range of temperatures (from -20 °C to 50 °C) and pH values (pH 3-pH 12) and a narrow host range against . Potent antimicrobial and antibiofilm activities were observed when the phage was tested against a highly susceptible bacterial isolate. These encouraging results open the door to new therapeutic opportunities in the fight against resilient biofilm-associated infections caused by .
Staphylococcus epidermidis has emerged as the most important pathogen in infections related to indwelling medical devices, and although these infections are not life-threatening, their frequency and the fact that they are extremely difficult to treat represent a serious burden on the public health system. Treatment is complicated by specific antibiotic resistance genes and the formation of biofilms. Hence, novel therapeutic strategies are needed to fight these infections. A novel bacteriophage CUB-EPI_14 specific to the bacterial species S. epidermidis was isolated from sewage and characterized genomically and phenotypically. Its genome contains a total of 46,098 bp and 63 predicted genes, among which some have been associated with packaging and lysis-associated proteins, structural proteins, or DNA- and metabolism-associated proteins. No lysogeny-associated proteins or known virulence proteins were identified in the phage genome. CUB-EPI_14 showed stability over a wide range of temperatures (from −20 °C to 50 °C) and pH values (pH 3–pH 12) and a narrow host range against S. epidermidis. Potent antimicrobial and antibiofilm activities were observed when the phage was tested against a highly susceptible bacterial isolate. These encouraging results open the door to new therapeutic opportunities in the fight against resilient biofilm-associated infections caused by S. epidermidis.
Author Fanaei Pirlar, Rima
Trampuz, Andrej
Gonzalez Moreno, Mercedes
Wagemans, Jeroen
Lavigne, Rob
Ponce Benavente, Luis
AuthorAffiliation 1 Charité—Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Center for Musculoskeletal Surgery, Augustenburger Platz 1, 13353 Berlin, Germany; rima.fanaei@charite.de (R.F.P.); luis.ponce-benavente@charite.de (L.P.B.); andrej.trampuz@charite.de (A.T.)
2 Berlin Institute of Health at Charité, Universitätsmedizin Berlin, BIH Center for Regenerative Therapies (BCRT), Charitéplatz 1, 10117 Berlin, Germany
3 KU Leuven, Department of Biosystems, Kasteelpark Arenberg 21, 3001 Leuven, Belgium; jeroen.wagemans@kuleuven.be (J.W.); rob.lavigne@kuleuven.be (R.L.)
AuthorAffiliation_xml – name: 1 Charité—Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Center for Musculoskeletal Surgery, Augustenburger Platz 1, 13353 Berlin, Germany; rima.fanaei@charite.de (R.F.P.); luis.ponce-benavente@charite.de (L.P.B.); andrej.trampuz@charite.de (A.T.)
– name: 2 Berlin Institute of Health at Charité, Universitätsmedizin Berlin, BIH Center for Regenerative Therapies (BCRT), Charitéplatz 1, 10117 Berlin, Germany
– name: 3 KU Leuven, Department of Biosystems, Kasteelpark Arenberg 21, 3001 Leuven, Belgium; jeroen.wagemans@kuleuven.be (J.W.); rob.lavigne@kuleuven.be (R.L.)
Author_xml – sequence: 1
  givenname: Rima
  surname: Fanaei Pirlar
  fullname: Fanaei Pirlar, Rima
  organization: Berlin Institute of Health at Charité, Universitätsmedizin Berlin, BIH Center for Regenerative Therapies (BCRT), Charitéplatz 1, 10117 Berlin, Germany
– sequence: 2
  givenname: Jeroen
  orcidid: 0000-0002-2185-5724
  surname: Wagemans
  fullname: Wagemans, Jeroen
  organization: KU Leuven, Department of Biosystems, Kasteelpark Arenberg 21, 3001 Leuven, Belgium
– sequence: 3
  givenname: Luis
  surname: Ponce Benavente
  fullname: Ponce Benavente, Luis
  organization: Berlin Institute of Health at Charité, Universitätsmedizin Berlin, BIH Center for Regenerative Therapies (BCRT), Charitéplatz 1, 10117 Berlin, Germany
– sequence: 4
  givenname: Rob
  surname: Lavigne
  fullname: Lavigne, Rob
  organization: KU Leuven, Department of Biosystems, Kasteelpark Arenberg 21, 3001 Leuven, Belgium
– sequence: 5
  givenname: Andrej
  orcidid: 0000-0002-5219-2521
  surname: Trampuz
  fullname: Trampuz, Andrej
  organization: Berlin Institute of Health at Charité, Universitätsmedizin Berlin, BIH Center for Regenerative Therapies (BCRT), Charitéplatz 1, 10117 Berlin, Germany
– sequence: 6
  givenname: Mercedes
  orcidid: 0000-0003-3586-6544
  surname: Gonzalez Moreno
  fullname: Gonzalez Moreno, Mercedes
  organization: Berlin Institute of Health at Charité, Universitätsmedizin Berlin, BIH Center for Regenerative Therapies (BCRT), Charitéplatz 1, 10117 Berlin, Germany
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35746811$$D View this record in MEDLINE/PubMed
BookMark eNpdkktv1DAQgC1URB9w4A-gSFzgsGDHdmxfkLYVj0oVHApHZDnjya5XSRxs76L994RuWbWcZjTz6dNoZs7JyRhHJOQlo-84N_T9jgnaMC7oE3LGjDELYZg8eZCfkvOcN5Q2jaHqGTnlUolGM3ZGfn6NO-yrSwcFU4jT2q2wup0QQhegcisXxlyq2-Km9b6PEAG2ucIpeExD8CFXbvTV71DW1XIsoQ2xC_1QLaGEXSj75-Rp5_qML-7jBfnx6eP3qy-Lm2-fr6-WNwsQvC6LtpW1955i7ZFqACaVoV4raGQrJICqa5TMNV4Aa5ACa2vupea1oFoa1fALcn3w-ug2dkphcGlvowv2rhDTyrpUAvRoUQmUIHnjtROKC6fb1gupGfVtx-5cHw6uadsO6AHHklz_SPq4M4a1XcWdNTWnjMlZ8OZekOKvLeZih5AB-96NGLfZ1vPmKZea0hl9_R-6ids0zquaKWW0MkzUM_X2QEGKOSfsjsMwav8-gD0-wMy-ejj9kfx3cf4HonGtZw
CitedBy_id crossref_primary_10_1128_msphere_00524_22
crossref_primary_10_1080_10408398_2023_2246554
crossref_primary_10_3389_fcimb_2023_1169135
crossref_primary_10_3390_pharmaceutics14102216
crossref_primary_10_1016_j_mib_2024_102434
crossref_primary_10_3390_v15122287
crossref_primary_10_3390_vaccines10122112
crossref_primary_10_3390_v15051042
crossref_primary_10_1128_mbio_01990_23
crossref_primary_10_1016_j_mran_2023_100249
Cites_doi 10.1186/1471-2164-13-228
10.1371/journal.pcbi.1005595
10.1093/bioinformatics/btr039
10.1016/S0378-1097(04)00041-2
10.1128/AEM.03560-14
10.1111/j.1365-2672.2011.04989.x
10.1038/s41564-018-0230-7
10.7150/ijbs.60551
10.1371/journal.pone.0206278
10.1093/nar/gkw1017
10.1101/2020.07.11.198606
10.1016/j.ijantimicag.2020.106200
10.3390/antibiotics10020175
10.1093/bioinformatics/btx157
10.1002/mbo3.558
10.4161/bact.1.2.14590
10.1038/s41467-021-27037-6
10.1099/vir.0.060590-0
10.1002/9781119720676.ch5
10.22203/eCM.v039a13
10.1016/S0022-2836(05)80360-2
10.1128/JCM.03617-13
10.1186/s12864-016-3018-2
10.1038/ijos.2014.65
10.1038/srep08365
10.1038/nmeth.2089
10.1038/s41598-017-07910-5
10.1093/nar/gky448
10.1016/j.resmic.2014.09.012
10.1007/s00284-010-9659-5
10.1016/j.resmic.2018.05.010
10.3389/fcimb.2021.798563
10.1038/nprot.2015.053
10.3390/v5030806
10.1073/pnas.2023202118
10.1038/nrmicro2182
10.1093/femsmc/xtab003
10.3389/fmicb.2019.01971
10.3390/v12101076
10.3389/fmicb.2018.02348
10.1101/2020.07.05.188268
10.1128/genomeA.00549-14
ContentType Journal Article
Copyright 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2022 by the authors. 2022
Copyright_xml – notice: 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2022 by the authors. 2022
DBID CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
3V.
7U9
7X7
7XB
88E
8FE
8FH
8FI
8FJ
8FK
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
FYUFA
GHDGH
GNUQQ
H94
HCIFZ
K9.
LK8
M0S
M1P
M7P
PIMPY
PQEST
PQQKQ
PQUKI
PRINS
7X8
5PM
DOA
DOI 10.3390/v14061340
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
ProQuest Central (Corporate)
Virology and AIDS Abstracts
ProQuest - Health & Medical Complete保健、医学与药学数据库
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
ProQuest Natural Science Collection
ProQuest One Community College
ProQuest Central
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection (Proquest) (PQ_SDU_P3)
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
Health & Medical Collection (Alumni Edition)
PML(ProQuest Medical Library)
Biological Science Database
Publicly Available Content Database
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
Publicly Available Content Database
ProQuest Central Student
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
ProQuest Central China
ProQuest Central
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Biological Science Collection
AIDS and Cancer Research Abstracts
ProQuest Medical Library (Alumni)
Virology and AIDS Abstracts
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList
MEDLINE

Publicly Available Content Database
CrossRef
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 4
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
Public Health
EISSN 1999-4915
ExternalDocumentID oai_doaj_org_article_e74e5c536d8a4734a8bbd45810dbf176
10_3390_v14061340
35746811
Genre Research Support, Non-U.S. Gov't
Journal Article
GeographicLocations United States--US
Germany
GeographicLocations_xml – name: United States--US
– name: Germany
GrantInformation_xml – fundername: JPIAMR: Cross-border research project ANTI-BIOLAB
  grantid: 40AR40_185917
– fundername: PRO-IMPLANT Foundation
– fundername: the German Research Foundation (DFG)
– fundername: the Open Access Publication Fund of Charité—Universitätsmedizin Berlin
GroupedDBID ---
2WC
3V.
53G
5VS
7X7
88E
8FE
8FH
8FI
8FJ
A8Z
AADQD
AAFWJ
AAHBH
ABDBF
ABUWG
AFKRA
AFPKN
AFZYC
ALIPV
ALMA_UNASSIGNED_HOLDINGS
BBNVY
BENPR
BHPHI
BPHCQ
BVXVI
CCPQU
CGR
CUY
CVF
DIK
E3Z
EBD
ECM
EIF
ESTFP
ESX
FYUFA
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IHR
ISR
ITC
KQ8
LK8
M1P
M48
M7P
MODMG
M~E
NPM
O5R
O5S
OK1
PGMZT
PIMPY
PQQKQ
PROAC
PSQYO
RIG
RPM
TR2
TUS
UKHRP
AAYXX
CITATION
7U9
7XB
8FK
AZQEC
DWQXO
GNUQQ
H94
K9.
PQEST
PQUKI
PRINS
7X8
5PM
ID FETCH-LOGICAL-c432t-bb52ddd0e2de08cc15790d87c65b45cc722e51a6d4c16e0c1b23d583240859763
IEDL.DBID RPM
ISSN 1999-4915
IngestDate Tue Oct 22 15:12:27 EDT 2024
Tue Sep 17 21:32:24 EDT 2024
Fri Aug 16 03:36:52 EDT 2024
Sun Oct 27 13:56:35 EDT 2024
Fri Aug 23 04:31:42 EDT 2024
Sat Nov 02 12:28:19 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 6
Keywords novel bacteriophage species
Staphylococcus epidermidis
biofilm-associated infection
whole-genome sequencing
isothermal microcalorimetry
Language English
License Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c432t-bb52ddd0e2de08cc15790d87c65b45cc722e51a6d4c16e0c1b23d583240859763
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0002-2185-5724
0000-0003-3586-6544
0000-0002-5219-2521
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9230115/
PMID 35746811
PQID 2679879142
PQPubID 2032319
ParticipantIDs doaj_primary_oai_doaj_org_article_e74e5c536d8a4734a8bbd45810dbf176
pubmedcentral_primary_oai_pubmedcentral_nih_gov_9230115
proquest_miscellaneous_2681035800
proquest_journals_2679879142
crossref_primary_10_3390_v14061340
pubmed_primary_35746811
PublicationCentury 2000
PublicationDate 20220620
PublicationDateYYYYMMDD 2022-06-20
PublicationDate_xml – month: 6
  year: 2022
  text: 20220620
  day: 20
PublicationDecade 2020
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
– name: Basel
PublicationTitle Viruses
PublicationTitleAlternate Viruses
PublicationYear 2022
Publisher MDPI AG
MDPI
Publisher_xml – name: MDPI AG
– name: MDPI
References Melo (ref_40) 2014; 95
Tisza (ref_31) 2021; 118
Elsener (ref_38) 2021; 12
ref_14
ref_36
Tkhilaishvili (ref_30) 2018; 169
ref_34
ref_11
ref_10
Altschul (ref_19) 1990; 215
Joensen (ref_37) 2014; 52
Wattam (ref_18) 2017; 45
ref_17
Koskella (ref_9) 2013; 5
ref_15
Sutherland (ref_42) 2004; 232
Lee (ref_5) 2018; 3
Espadinha (ref_3) 2019; 10
Wang (ref_28) 2020; 56
Wang (ref_26) 2016; 7
(ref_39) 2010; 61
Garneau (ref_35) 2017; 7
Kelley (ref_24) 2015; 10
Onsea (ref_7) 2020; 39
Sullivan (ref_25) 2011; 27
Abedon (ref_8) 2011; 1
Schneider (ref_16) 2012; 9
ref_21
Nabergoj (ref_29) 2018; 7
Otto (ref_2) 2009; 7
Nishimura (ref_20) 2017; 33
Campelo (ref_41) 2018; 9
Potter (ref_23) 2018; 46
Melo (ref_32) 2014; 165
Brettin (ref_22) 2015; 5
Vandenheuvel (ref_13) 2015; 81
Valente (ref_12) 2021; 2
Li (ref_43) 2021; 17
Viazis (ref_27) 2011; 110
Aswani (ref_33) 2014; 2
Oliveira (ref_1) 2021; 11
Wu (ref_4) 2015; 7
ref_6
References_xml – ident: ref_11
  doi: 10.1186/1471-2164-13-228
– ident: ref_17
  doi: 10.1371/journal.pcbi.1005595
– volume: 27
  start-page: 1009
  year: 2011
  ident: ref_25
  article-title: Easyfig: A genome comparison visualizer
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btr039
  contributor:
    fullname: Sullivan
– volume: 232
  start-page: 1
  year: 2004
  ident: ref_42
  article-title: The interaction of phage and biofilms
  publication-title: FEMS Microbiol. Lett.
  doi: 10.1016/S0378-1097(04)00041-2
  contributor:
    fullname: Sutherland
– volume: 81
  start-page: 3336
  year: 2015
  ident: ref_13
  article-title: Two Phages, phiIPLA-RODI and phiIPLA-C1C, Lyse Mono- and Dual-Species Staphylococcal Biofilms
  publication-title: Appl. Environ. Microbiol.
  doi: 10.1128/AEM.03560-14
  contributor:
    fullname: Vandenheuvel
– volume: 110
  start-page: 1323
  year: 2011
  ident: ref_27
  article-title: Isolation and characterization of lytic bacteriophages against enterohaemorrhagic Escherichia coli
  publication-title: J. Appl. Microbiol.
  doi: 10.1111/j.1365-2672.2011.04989.x
  contributor:
    fullname: Viazis
– volume: 3
  start-page: 1175
  year: 2018
  ident: ref_5
  article-title: Global spread of three multidrug-resistant lineages of Staphylococcus epidermidis
  publication-title: Nat. Microbiol.
  doi: 10.1038/s41564-018-0230-7
  contributor:
    fullname: Lee
– volume: 17
  start-page: 3573
  year: 2021
  ident: ref_43
  article-title: A combination therapy of Phages and Antibiotics: Two is better than one
  publication-title: Int. J. Biol. Sci.
  doi: 10.7150/ijbs.60551
  contributor:
    fullname: Li
– ident: ref_15
  doi: 10.1371/journal.pone.0206278
– volume: 45
  start-page: D535
  year: 2017
  ident: ref_18
  article-title: Improvements to PATRIC, the all-bacterial Bioinformatics Database and Analysis Resource Center
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkw1017
  contributor:
    fullname: Wattam
– ident: ref_36
  doi: 10.1101/2020.07.11.198606
– volume: 56
  start-page: 106200
  year: 2020
  ident: ref_28
  article-title: Bacteriophage–antibiotic combinations against ciprofloxacin/ceftriaxone-resistant Escherichia coli in vitro and in an experimental Galleria mellonella model
  publication-title: Int. J. Antimicrob. Agents
  doi: 10.1016/j.ijantimicag.2020.106200
  contributor:
    fullname: Wang
– ident: ref_10
  doi: 10.3390/antibiotics10020175
– volume: 33
  start-page: 2379
  year: 2017
  ident: ref_20
  article-title: ViPTree: The viral proteomic tree server
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btx157
  contributor:
    fullname: Nishimura
– volume: 7
  start-page: e00558
  year: 2018
  ident: ref_29
  article-title: Effect of bacterial growth rate on bacteriophage population growth rate
  publication-title: Microbiologyopen
  doi: 10.1002/mbo3.558
  contributor:
    fullname: Nabergoj
– volume: 1
  start-page: 111
  year: 2011
  ident: ref_8
  article-title: Pros and cons of phage therapy
  publication-title: Bacteriophage
  doi: 10.4161/bact.1.2.14590
  contributor:
    fullname: Abedon
– volume: 12
  start-page: 6965
  year: 2021
  ident: ref_38
  article-title: Multi-species host range of staphylococcal phages isolated from wastewater
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-021-27037-6
  contributor:
    fullname: Elsener
– volume: 95
  start-page: 506
  year: 2014
  ident: ref_40
  article-title: Isolation and characterization of a new Staphylococcus epidermidis broad-spectrum bacteriophage
  publication-title: J. Gen. Virol.
  doi: 10.1099/vir.0.060590-0
  contributor:
    fullname: Melo
– ident: ref_6
  doi: 10.1002/9781119720676.ch5
– volume: 39
  start-page: 193
  year: 2020
  ident: ref_7
  article-title: Bacteriophage therapy as a treatment strategy for orthopaedic-device-related infections: Where do we stand?
  publication-title: Eur. Cells Mater.
  doi: 10.22203/eCM.v039a13
  contributor:
    fullname: Onsea
– volume: 215
  start-page: 403
  year: 1990
  ident: ref_19
  article-title: Basic local alignment search tool
  publication-title: J. Mol. Biol.
  doi: 10.1016/S0022-2836(05)80360-2
  contributor:
    fullname: Altschul
– volume: 52
  start-page: 1501
  year: 2014
  ident: ref_37
  article-title: Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli
  publication-title: J. Clin. Microbiol.
  doi: 10.1128/JCM.03617-13
  contributor:
    fullname: Joensen
– ident: ref_34
  doi: 10.1186/s12864-016-3018-2
– volume: 7
  start-page: 1
  year: 2015
  ident: ref_4
  article-title: Strategies for combating bacterial biofilm infections
  publication-title: Int. J. Oral Sci.
  doi: 10.1038/ijos.2014.65
  contributor:
    fullname: Wu
– volume: 5
  start-page: 8365
  year: 2015
  ident: ref_22
  article-title: RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes
  publication-title: Sci. Rep.
  doi: 10.1038/srep08365
  contributor:
    fullname: Brettin
– volume: 7
  start-page: 934
  year: 2016
  ident: ref_26
  article-title: SLPW: A Virulent Bacteriophage Targeting Methicillin-Resistant Staphylococcus aureus In vitro and In vivo
  publication-title: Front. Microbiol.
  contributor:
    fullname: Wang
– volume: 9
  start-page: 671
  year: 2012
  ident: ref_16
  article-title: NIH Image to ImageJ: 25 years of image analysis
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.2089
  contributor:
    fullname: Schneider
– volume: 7
  start-page: 8292
  year: 2017
  ident: ref_35
  article-title: PhageTerm: A tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-017-07910-5
  contributor:
    fullname: Garneau
– volume: 46
  start-page: W200
  year: 2018
  ident: ref_23
  article-title: HMMER web server: 2018 update
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gky448
  contributor:
    fullname: Potter
– volume: 165
  start-page: 679
  year: 2014
  ident: ref_32
  article-title: Characterization of Staphylococcus epidermidis phage vB_SepS_SEP9-a unique member of the Siphoviridae family
  publication-title: Res. Microbiol.
  doi: 10.1016/j.resmic.2014.09.012
  contributor:
    fullname: Melo
– volume: 61
  start-page: 601
  year: 2010
  ident: ref_39
  article-title: Isolation and Characterization of Bacteriophages Infecting Staphylococcus epidermidis
  publication-title: Curr. Microbiol.
  doi: 10.1007/s00284-010-9659-5
– volume: 169
  start-page: 515
  year: 2018
  ident: ref_30
  article-title: Real-time assessment of bacteriophage T3-derived antimicrobial activity against planktonic and biofilm-embedded Escherichia coli by isothermal microcalorimetry
  publication-title: Res. Microbiol.
  doi: 10.1016/j.resmic.2018.05.010
  contributor:
    fullname: Tkhilaishvili
– volume: 11
  start-page: 798563
  year: 2021
  ident: ref_1
  article-title: Fighting Staphylococcus epidermidis Biofilm-Associated Infections: Can Iron Be the Key to Success?
  publication-title: Front. Cell. Infect. Microbiol.
  doi: 10.3389/fcimb.2021.798563
  contributor:
    fullname: Oliveira
– volume: 10
  start-page: 845
  year: 2015
  ident: ref_24
  article-title: The Phyre2 web portal for protein modeling, prediction and analysis
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2015.053
  contributor:
    fullname: Kelley
– volume: 5
  start-page: 806
  year: 2013
  ident: ref_9
  article-title: Understanding bacteriophage specificity in natural microbial communities
  publication-title: Viruses
  doi: 10.3390/v5030806
  contributor:
    fullname: Koskella
– volume: 118
  start-page: e2023202118
  year: 2021
  ident: ref_31
  article-title: A catalog of tens of thousands of viruses from human metagenomes reveals hidden associations with chronic diseases
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.2023202118
  contributor:
    fullname: Tisza
– volume: 7
  start-page: 555
  year: 2009
  ident: ref_2
  article-title: Staphylococcus epidermidis--the ‘accidental’ pathogen
  publication-title: Nat. Rev. Microbiol.
  doi: 10.1038/nrmicro2182
  contributor:
    fullname: Otto
– volume: 2
  start-page: xtab003
  year: 2021
  ident: ref_12
  article-title: Isolation and characterization of bacteriophages from the human skin microbiome that infect Staphylococcus epidermidis
  publication-title: FEMS Microbes
  doi: 10.1093/femsmc/xtab003
  contributor:
    fullname: Valente
– volume: 10
  start-page: 1971
  year: 2019
  ident: ref_3
  article-title: Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages
  publication-title: Front. Microbiol.
  doi: 10.3389/fmicb.2019.01971
  contributor:
    fullname: Espadinha
– ident: ref_14
  doi: 10.3390/v12101076
– volume: 9
  start-page: 2348
  year: 2018
  ident: ref_41
  article-title: Analysis of Different Parameters Affecting Diffusion, Propagation and Survival of Staphylophages in Bacterial Biofilms
  publication-title: Front. Microbiol.
  doi: 10.3389/fmicb.2018.02348
  contributor:
    fullname: Campelo
– ident: ref_21
  doi: 10.1101/2020.07.05.188268
– volume: 2
  start-page: e00549-14
  year: 2014
  ident: ref_33
  article-title: Complete Genome Sequence of a Staphylococcus epidermidis Bacteriophage Isolated from the Anterior Nares of Humans
  publication-title: Genome Announc.
  doi: 10.1128/genomeA.00549-14
  contributor:
    fullname: Aswani
SSID ssj0066907
Score 2.4139864
Snippet has emerged as the most important pathogen in infections related to indwelling medical devices, and although these infections are not life-threatening, their...
Staphylococcus epidermidis has emerged as the most important pathogen in infections related to indwelling medical devices, and although these infections are...
Staphylococcus epidermidis has emerged as the most important pathogen in infections related to indwelling medical devices, and although these infections are...
SourceID doaj
pubmedcentral
proquest
crossref
pubmed
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage 1340
SubjectTerms Adsorption
Anti-Bacterial Agents - therapeutic use
Antibiotic resistance
Antibiotics
Bacteria
Bacterial infections
Bacteriophages - genetics
biofilm-associated infection
Biofilms
Efficiency
Genomes
Host range
Humans
Infections
isothermal microcalorimetry
Lysis
Lysogeny
Medical equipment
novel bacteriophage species
Pathogens
pH effects
Phages
Polyethylene glycol
Public health
Sewage
Staphylococcal Infections - microbiology
Staphylococcus epidermidis
Structural proteins
Transmission electron microscopy
Transplants & implants
Virulence
whole-genome sequencing
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3dSxwxEA8iCL6Uttp2rS2p-LqYZPOx-3gWRQr6VMEXWZJJth60u-LdCf73ndncHXel0Je-bkKYnUlmfpOP3zB2qoRToGxXhtj4UnedLUNjYonQKOGcUgYivUa-vrFXt_rbnbnbKPVFd8IyPXBW3FlyOhkwlY21167Svg4halNLEUMnXSbbFs0qmco-2FLOl3mEKkzqz57lGLdoh2Mj-owk_X9Dln9ekNyIOJev2aslVOSTLOIbtpP6t2wvF498OWD3N8Nz-snPM93y8PiAnoGP5eS7KXD_A1P-2ZwjmERFYsQaABYznqggLNo2Tmfc95HTNiyf9PRwhGp3_-ITyOUkDtnt5cX3r1flslhCCbpS8zIEo2KMIilUcg0gjWtErB1YE7QBcEolI72NGqRNAmRQVTR1lSnO0Mu8Y7v90KcPjGsThYwduJSSNs4H26XQ1Y2SHkSsRMFOVkpsHzMnRou5BGm6XWu6YOek3nUHorEeP6Bx26Vx238Zt2DHK-O0y7U1axUdHLlGalWwL-tmXBV01OH7NCyoD45BJ7wox_tsy7UklXEam2XB3JaVt0TdbumnDyPzNqJhgtBH_-PfPrJ9RU8phEVPdcx250-L9AkBzjx8Hufyb0aU_DQ
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: ProQuest Central
  dbid: BENPR
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3ra9RAEB_0iiAU0fqKVlnFr6HZzT5yn-ROWorgIWKhXyTsK-1BTc7eXaH_vTPZ3NkT8Wt2CcPM7jx35gfwQRRGeKGb3IWxzWXT6NyNVcjRNYp4poTygbqRv8z06Zn8fK7Oh4TbcnhWudGJvaIOnacc-ZGgcoEZcyk-Ln7lhBpF1dUBQuM-7AmMFMQI9qbHs6_fNrpYU-yX5gmVGNwf3fDeflGm444V6of1_8vD_Puh5B3Lc_IYHg0uI5skGT-Be7E9gAcJRPL2APZT5o2lhqKn8GPW3cQrNk1jmLvFJWoM1sPMN7jLXtg5eoQMnUxkMFqyzvv1kkUCikWZh_mS2TYwSs-ySUsNJYTp_ZNNfIKZeAZnJ8ffP53mA4hC7mUpVrlzSoQQiiiQ-ZX3XJlxESrjtXJSeW-EiIpbHaTnOhaeO1EGVZVp9Blqn-cwars2vgQmVSh4aLyJMUplrNNNdE01Ftz6IpRFBu83TK0XaVZGjTEGcb7ecj6DKbF7u4HGW_cfuuuLergtdTQyKq9KHSorTSlt5VyQquJFcA03OoPDjbDq4c4t6z8nJIN322W8LVQCsW3s1rQH_0GVX6TjRZLtlpJSGYnLPAOzI_UdUndX2vllP5EbvWRyrV_9n6zX8FBQ80ShUTcdwmh1vY5v0KVZubfDuf0NRqL5-w
  priority: 102
  providerName: ProQuest
– databaseName: Scholars Portal Journals: Open Access
  dbid: M48
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB5VRaBeEOUZKMggroHY8SM5VNW2oqqQ6ImVekGRX2lXKknZR0X_PTPJJiKoJ66xE1kzY883sf19AB9FZoQXuk5dKG0q61qnrlQhRWgUMaaE8oFuI38712dz-fVCXezAoLG5NeDq3tKO9KTmy-tPv3_dHeGEP6SKE0v2z7e8y0oSK_cHgvi46ASfHDcTNBWAPanQtPsePMqVkbrgfJKVOvL--xDnvwcn_8pEp0_g8RZCslnv833Yic1TeNiLSt49gx_n7W28Zsc9DXN7c4UrButk5uuFZ_bSLhARMgSZaGDMZK33mxWLJBSLPg-LFbNNYPR7ls0aulBCmt4_2cz3MhPPYX765fvJWboVUUi9zMU6dU6JEEIWBRq_8J4rU2ahMF4rJ5X3RoiouNVBeq5j5rkTeVBF3lOf4erzAnabtomvgEkVMh5qb2KMUhnrdB1dXZSCW5-FPEvgw2DE6qbnyqiwxiCjV6PREzgm844diN66e9AuL6vtbKmikVF5letQWGlyaQvnglQFz4KrudEJHAzOqYaQqQRtKJmSS5HA-7EZZwttgdgmthvqg9-gnV8cx8vel-NIhlhIwEy8PBnqtKVZXHWM3IiSCVq__u8338CeoHsVmcZl6wB218tNfItoZ-3edbH8B-hDAkw
  priority: 102
  providerName: Scholars Portal
Title Novel Bacteriophage Specific against Staphylococcus epidermidis and with Antibiofilm Activity
URI https://www.ncbi.nlm.nih.gov/pubmed/35746811
https://www.proquest.com/docview/2679879142
https://search.proquest.com/docview/2681035800
https://pubmed.ncbi.nlm.nih.gov/PMC9230115
https://doaj.org/article/e74e5c536d8a4734a8bbd45810dbf176
Volume 14
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnR1da9sw8Gg7BnsZ-663Lmhjr24sWR_2Y1LalUFCGSvkZRjrJLeBxg5NUui_78mOwzL2tBc9WJI57k73Id0HwDeRGIFCV7F1eRnLqtKxzZWLyTTyxFNCoQvZyJOpvryWP2ZqdgCqz4Vpg_bRzk_ru8VpPb9tYyuXCxz2cWLDq8kZGSXBkhkewiExaO-id-JXB3evKyGUkj8_fOCtypKh5VuqjNQZ53s6qC3V_y_78u8wyT_0zsUreLk1GNmoA-w1HPj6DTzvWkg-voXf0-bB37FxV3S5Wd6SfGBtU_lqjqy8Icd_tWZkUhI6SW81iJsV86EtLFHYzVesrB0Ll7FsVIf0kdDBe8FG2DWVeAfXF-e_zi7jbcuEGGUq1rG1SjjnEi8I1RkiVyZPXGZQKysVohHCK15qJ5FrnyC3InUqS7tCZyRr3sNR3dT-GJhULuGuQuO9l8qUVlfeVlkueImJS5MIvvZILJZdZYyCPIqA9GKH9AjGAb27BaGYdfuhub8ptiQtvJFeoUq1y0ppUllm1jqpMp44W3GjIzjpiVNsT9iqEOH5yORcigi-7KbpbIQHj7L2zSasoX-Ed16C40NHyx0kPS9EYPaovAfq_gyxY1t_e8t-H_975yd4IUIWRaJJSJ3A0fp-4z-TbbO2A-LomRnAs_H59OrnoL0hoPH7jNM4kdmg5fUnC40BwA
link.rule.ids 230,315,730,783,787,867,888,2109,2228,12070,21402,24332,27938,27939,31733,31734,33758,33759,43324,43819,53806,53808,74081,74638
linkProvider National Library of Medicine
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3da9RAEF-0IhZEtNoaW3UVX0Ozm_1Insq1tJza3lML9yJhv9IeaHL27gr-985kc7En4mt2CcPM7nzu_IaQTzzT3HFVp9aXJhV1rVJbSp-CaxTgTHHpPHYjX0zU-Ep8mcppn3Bb9M8q1zqxU9S-dZgjP-RYLtAlE_xo_jPFqVFYXe1HaDwkjxCHC7Hz9XQIuBRGfhFNKIfQ_vCOddYL8xz3bFAH1f8v__LvZ5L37M7Zc_KsdxjpKEr4BXkQmh3yOI6Q_LVDnsa8G43tRC_Jt0l7F77T4wjC3M5vQF_Qbsh8DbvMtZmBP0jBxQT2gh1rnVstaMAxsSBxP1tQ03iKyVk6arCdBCd6_6AjF4dMvCJXZ6eXJ-O0H6GQOpHzZWqt5N77LHBgfeEck7rMfKGdklZI5zTnQTKjvHBMhcwxy3MvizwCn4Hu2SVbTduE14QK6TPma6dDCEJqY1UdbF2UnBmX-TxLyMc1U6t5RMqoIMJAzlcD5xNyjOweNiC4dfehvb2u-rtSBS2CdDJXvjBC58IU1nohC5Z5WzOtEnKwFlbV37hF9ed8JOTDsAx3BQsgpgntCvfAP7DuC3TsRdkOlORSC1hmCdEbUt8gdXOlmd10eNzgI6Nj_eb_ZL0nT8aXF-fV-efJ132yzbGNIlOgpQ7I1vJ2Fd6Cc7O077oT_Bv_FvuG
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfR1ra9RAcNGKUpCiVdto1VX8Gi672UfySa7qUV-HHyzcFwn7Sntgk7N3V_DfO5PNpT0Rv2aXMMzMzvtByBueae64qlPrS5OKulapLaVPwTQKwFNcOo_dyF-n6uRUfJrJWV__tOzLKjcysRPUvnUYIx9xTBfokgk-qvuyiG_vJ28Xv1LcIIWZ1n6dxm1yRwtQdMDbejY4Xwq9wDhZKAc3f3TFOk2GMY8b-qgb2_8vW_PvkskbOmjygOz1xiMdR2o_JLdCs0_uxnWSv_fJ_RiDo7G16BH5MW2vwk96HAcyt4tzkB20Wzhfwy1zZuZgG1IwNwHVoNNa59ZLGnBlLFDfz5fUNJ5ioJaOG2wtwe3eF3Ts4sKJx-R08uH7u5O0X6eQOpHzVWqt5N77LHAgQ-Eck7rMfKGdklZI5zTnQTKjvHBMhcwxy3MvizwOQQM59ITsNG0TDgkV0mfM106HEITUxqo62LooOTMu83mWkNcbpFaLODWjAm8DMV8NmE_IMaJ7uICDrrsP7eVZ1b-bKmgRpJO58oUROhemsNYLWbDM25pplZCjDbGq_vUtq2teScir4RjeDSZDTBPaNd6Bf2AOGOA4iLQdIMmlFnDMEqK3qL4F6vZJMz_vZnODvYxG9tP_g_WS3APmrb58nH5-RnY5dlRkCgTWEdlZXa7Dc7BzVvZFx8B_AJYM_7s
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Novel+Bacteriophage+Specific+against+Staphylococcus+epidermidis+and+with+Antibiofilm+Activity&rft.jtitle=Viruses&rft.au=Fanaei+Pirlar%2C+Rima&rft.au=Wagemans%2C+Jeroen&rft.au=Ponce+Benavente%2C+Luis&rft.au=Lavigne%2C+Rob&rft.date=2022-06-20&rft.pub=MDPI&rft.eissn=1999-4915&rft.volume=14&rft.issue=6&rft_id=info:doi/10.3390%2Fv14061340&rft_id=info%3Apmid%2F35746811&rft.externalDBID=PMC9230115
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1999-4915&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1999-4915&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1999-4915&client=summon