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Trudy Wassenaar Molecular Microbiology and Genomics Consultants Tannestrasse 7 55576 Zotzenheim Germany

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David Ussery

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Lene Nielsen University of Copenhagen Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences Copenhagen Denmark

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Hanne Ingmer University of Copenhagen Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences Copenhagen Denmark

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The qac genes of Staphylococcus species encode multidrug efflux pumps: membrane proteins that export toxic molecules and thus increase tolerance to a variety of compounds such as disinfecting agents, including quaternary ammonium compounds (for which they are named), intercalating dyes and some antibiotics. In Stapylococcus species, six different plasmid-encoded Qac efflux pumps have been described, and they belong to two major protein families. QacA and QacB are members of the Major Facilitator Superfamily, while QacC, QacG, QacH, and QacJ all belong to the Small Multidrug Resistance (SMR) family. Not all SMR proteins are called Qac and the reverse is also true, which has caused confusion in the literature and in gene annotations. The discovery of qac genes and their presence in various staphylococcal populations is briefly reviewed. A sequence comparison revealed that some of the PCR primers described in the literature for qac detection may miss particular qac genes due to lack of DNA conservation. Despite their resemblance in substrate specificity, the Qac proteins belonging to the two protein families have little in common. QacA and QacB are highly conserved in Staphylococcus species, while qacA was also detected in Enterococcus faecalis, suggesting that these plasmid-born genes have spread across bacterial genera. Nevertheless, these qacA and qacB genes are quite dissimilar to their closest homologues in other organisms. In contrast, SMR-type Qac proteins display considerable sequence variation, despite their short length, even within the Staphylococcus genus. Phylogenetic analysis of these genes identified similarity to a large number of other SMR members, found in staphylococci as well as in other genera. A number of phylogenetic trees of SMR Qac proteins are presented here, starting with genes present in S. aureus and S. epidermidis, and extending this to related genes found in other species of this genus, and finally to genes found in other genera.

  • Lyon BR, Skurray R: Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol Rev 51, 88–134 (1987)

    Skurray R , 'Antimicrobial resistance of Staphylococcus aureus: genetic basis ' (1987 ) 51 Microbiol Rev : 88 -134 .

    • Search Google Scholar
  • Littlejohn TG, DiBerardino D, Messerotti LJ, Spiers SJ, Skurray RA: Structure and evolution of a family of genes encoding antiseptic and disinfectant resistance in Staphylococcus aureus. Gene 101, 59–66 (1991)

    Skurray RA , 'Structure and evolution of a family of genes encoding antiseptic and disinfectant resistance in Staphylococcus aureus ' (1991 ) 101 Gene : 59 -66 .

    • Search Google Scholar
  • Putman M, van Veen HW, Konings WN: Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Rev 64, 672–693 (2000)

    Konings WN , 'Molecular properties of bacterial multidrug transporters ' (2000 ) 64 Microbiol Mol Biol Rev : 672 -693 .

    • Search Google Scholar
  • Buffet-Bataillon S, Tattevin P, Bonnaure-Mallet M, Jolivet-Gougeon A: Emergence of resistance to antibacterial agents: the role of quaternary ammonium compounds — a critical review. Int J Antimicrob Agents 39, 381–389 (2012)

    Jolivet-Gougeon A , 'Emergence of resistance to antibacterial agents: the role of quaternary ammonium compounds — a critical review ' (2012 ) 39 Int J Antimicrob Agents : 381 -389 .

    • Search Google Scholar
  • Furi L, Ciusa ML, Knight D, Di Lorenzo V, Tocci N, Cirasola D, Aragones L, Coelho JR, Freitas AT, Marchi E, Moce L, Visa P, Northwood JB, Viti C, Borghi E, Orefici G; BIOHYPO Consortium, Morrissey I, Oggioni MR: Evaluation of reduced susceptibility to quaternary ammonium compounds and bisbiguanides in clinical isolates and laboratory-generated mutants of Staphylococcus aureus. Antimicrob Agents Chemother 57, 3488–3497 (2013)

    Orefici G , 'Evaluation of reduced susceptibility to quaternary ammonium compounds and bisbiguanides in clinical isolates and laboratory-generated mutants of Staphylococcus aureus ' (2013 ) 57 Antimicrob Agents Chemother : 3488 -3497 .

    • Search Google Scholar
  • Costa SS, Viveiros M, Amaral L, Couto I: Multidrug Efflux Pumps in Staphylococcus aureus: an Update. Open Microbiol J 7, 59–71 (2013)

    Couto I , 'Multidrug Efflux Pumps in Staphylococcus aureus: an Update ' (2013 ) 7 Open Microbiol J : 59 -71 .

    • Search Google Scholar
  • Fuentes DE, Navarro CA, Tantaleán JC, Araya MA, Saavedra CP, Pérez JM, Calderón IL, Youderian PA, Mora GC, Vásquez CC: The product of the qacC gene of Staphylococcus epidermidis CH mediates resistance to beta-lactam antibiotics in gram-positive and gram-negative bacteria. Res Microbiol 156, 472–477 (2005)

    Vásquez CC , 'The product of the qacC gene of Staphylococcus epidermidis CH mediates resistance to beta-lactam antibiotics in gram-positive and gram-negative bacteria ' (2005 ) 156 Res Microbiol : 472 -477 .

    • Search Google Scholar
  • Nakaminami H, Noguchi N, Sasatsu M: Fluoroquinolone efflux by the plasmid-mediated multidrug efflux pump QacB variant QacBIII in Staphylococcus aureus. Antimicrob. Agents Chemother 54, 4107–4111 (2010)

    Sasatsu M , 'Fluoroquinolone efflux by the plasmid-mediated multidrug efflux pump QacB variant QacBIII in Staphylococcus aureus ' (2010 ) 54 Antimicrob. Agents Chemother : 4107 -4111 .

    • Search Google Scholar
  • Lowy FD: Staphylococcus aureus infections. N Engl J Med 339, 520–532 (1998)

    Lowy FD , 'Staphylococcus aureus infections ' (1998 ) 339 N Engl J Med : 520 -532 .

  • Taylor AR: Methicillin-resistant Staphylococcus aureus infections. Prim Care 40, 637–654 (2013)

    Taylor AR , 'Methicillin-resistant Staphylococcus aureus infections ' (2013 ) 40 Prim Care : 637 -654 .

    • Search Google Scholar
  • Uhlemann A-C, Otto M, Lowy FD, DeLeo FR: Evolution of community- and healthcare-associated methicillin-resistant Staphylococcus aureus. Infect Genet Evol 21, 563–574 (2014)

    DeLeo FR , 'Evolution of community- and healthcare-associated methicillin-resistant Staphylococcus aureus ' (2014 ) 21 Infect Genet Evol : 563 -574 .

    • Search Google Scholar
  • Fluit AC: Livestock-associated Staphylococcus aureus. Clin Microbiol Infect 18, 735–744 (2012)

    Fluit AC , 'Livestock-associated Staphylococcus aureus ' (2012 ) 18 Clin Microbiol Infect : 735 -744 .

    • Search Google Scholar
  • Otto M: Staphylococcus epidermidis — the “accidental” pathogen. Nat Rev Microbiol 7, 555–567 (2009)

    Otto M , 'Staphylococcus epidermidis — the “accidental” pathogen ' (2009 ) 7 Nat Rev Microbiol : 555 -567 .

    • Search Google Scholar
  • Vali L, Davies SE, Lai LLG, Dave J, Amyes SGB: Frequency of biocide resistance genes, antibiotic resistance and the effect of chlorhexidine exposure on clinical methicillin-resistant Staphylococcus aureus isolates. J Antimicrob Chemother 61(3), 524–532 (2008)

    Amyes SGB , 'Frequency of biocide resistance genes, antibiotic resistance and the effect of chlorhexidine exposure on clinical methicillin-resistant Staphylococcus aureus isolates ' (2008 ) 61 J Antimicrob Chemother : 524 -532 .

    • Search Google Scholar
  • Smith K, Gemmell CG, Hunter IS: The association between biocide tolerance and the presence or absence of qac genes among hospital-acquired and community-acquired MRSA isolates. J Antimicrob Chemother 61, 78–84 (2008)

    Hunter IS , 'The association between biocide tolerance and the presence or absence of qac genes among hospital-acquired and community-acquired MRSA isolates ' (2008 ) 61 J Antimicrob Chemother : 78 -84 .

    • Search Google Scholar
  • Cervinkova D, Babak V, Marosevic D, Kubikova I, Jaglic Z: The role of the qacA gene in mediating resistance to quaternary ammonium compounds. Microb Drug Resist 19, 160–167 (2013)

    Jaglic Z , 'The role of the qacA gene in mediating resistance to quaternary ammonium compounds ' (2013 ) 19 Microb Drug Resist : 160 -167 .

    • Search Google Scholar
  • Bay DC, Turner RJ: Diversity and evolution of the small multidrug resistance protein family. BMC Evol Biol 9, 140 (2009)

    Turner RJ , 'Diversity and evolution of the small multidrug resistance protein family ' (2009 ) 9 BMC Evol Biol : 140 -.

    • Search Google Scholar
  • Reddy VS, Shlykov MA, Castillo R, Sun EI, Saier MH: The major facilitator superfamily (MFS) revisited. FEBS J 279, 2022–2035 (2012)

    Saier MH , 'The major facilitator superfamily (MFS) revisited ' (2012 ) 279 FEBS J : 2022 -2035 .

    • Search Google Scholar
  • Johnston LH, Dyke KG: Ethidium bromide resistance, a new marker on the staphylococcal penicillinase plasmid. J Bacteriol 100, 1413–1414 (1969)

    Dyke KG , 'Ethidium bromide resistance, a new marker on the staphylococcal penicillinase plasmid ' (1969 ) 100 J Bacteriol : 1413 -1414 .

    • Search Google Scholar
  • Sasatsu M, Shima K, Shibata Y, Kono M: Nucleotide sequence of a gene that encodes resistance to ethidium bromide from a transferable plasmid in Staphylococcus aureus. Nucleic Acids Res 17, 10103 (1989)

    Kono M , 'Nucleotide sequence of a gene that encodes resistance to ethidium bromide from a transferable plasmid in Staphylococcus aureus ' (1989 ) 17 Nucleic Acids Res : 10103 -.

    • Search Google Scholar
  • Rouch DA, Cram DS, DiBerardino D, Littlejohn TG, Skurray RA: Efflux-mediated antiseptic resistance gene qacA from Staphylococcus aureus: common ancestry with tetracycline-and sugar-transport proteins. Mol Microbiol 4, 2051–62 (1990)

    Skurray RA , 'Efflux-mediated antiseptic resistance gene qacA from Staphylococcus aureus: common ancestry with tetracycline-and sugar-transport proteins ' (1990 ) 4 Mol Microbiol : 2051 -62 .

    • Search Google Scholar
  • Gillespie MT, Lyon BR, Skurray RA: Gentamicin and antiseptic resistance in epidemic methicillin-resistant Staphylococcus aureus. Lancet 1(8636), 503 (1989)

    Skurray RA , 'Gentamicin and antiseptic resistance in epidemic methicillin-resistant Staphylococcus aureus ' (1989 ) 1 Lancet : 503 -.

    • Search Google Scholar
  • Peters KM, Sharbeen G, Theis T, Skurray RA, Brown MH: Biochemical characterization of the multidrug regulator QacR distinguishes residues that are crucial to multidrug binding and induction of qacA transcription. Biochem 48, 9794–9800 (2009)

    Brown MH , 'Biochemical characterization of the multidrug regulator QacR distinguishes residues that are crucial to multidrug binding and induction of qacA transcription ' (2009 ) 48 Biochem : 9794 -9800 .

    • Search Google Scholar
  • Paulsen IT, Brown MH, Littlejohn TG, Mitchell BA, Skurray RA: Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: membrane topology and identification of residues involved in substrate specificity. Proc Natl Acad Sci USA 93, 3630–3635 (1996)

    Skurray RA , 'Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: membrane topology and identification of residues involved in substrate specificity ' (1996 ) 93 Proc Natl Acad Sci USA : 3630 -3635 .

    • Search Google Scholar
  • Grinius L, Dreguniene G, Goldberg EB, Liao CH, Projan SJ: A staphylococcal multidrug resistance gene product is a member of a new protein family. Plasmid 27, 119–129 (1992)

    Projan SJ , 'A staphylococcal multidrug resistance gene product is a member of a new protein family ' (1992 ) 27 Plasmid : 119 -129 .

    • Search Google Scholar
  • Grinius LL, Goldberg EB: Bacterial multidrug resistance is due to a single membrane protein which functions as a drug pump. J Biol Chem 269, 29998–30004 (1994)

    Goldberg EB , 'Bacterial multidrug resistance is due to a single membrane protein which functions as a drug pump ' (1994 ) 269 J Biol Chem : 29998 -30004 .

    • Search Google Scholar
  • Leelaporn A, Firth N, Paulsen IT, Hettiaratchi A, Skurray RA: Multidrug resistance plasmid pSK108 from coagulase-negative staphylococci; relationships to Staphylococcus aureus qacC plasmids. Plasmid 34, 62–67 (1995)

    Skurray RA , 'Multidrug resistance plasmid pSK108 from coagulase-negative staphylococci; relationships to Staphylococcus aureus qacC plasmids ' (1995 ) 34 Plasmid : 62 -67 .

    • Search Google Scholar
  • Schuldiner S: EmrE, a model for studying evolution and mechanism of ion-coupled transporters. Biochim Biophys Acta 1794, 748–762 (2009)

    Schuldiner S , 'EmrE, a model for studying evolution and mechanism of ion-coupled transporters ' (2009 ) 1794 Biochim Biophys Acta : 748 -762 .

    • Search Google Scholar
  • Poget SF, Harris R, Cahill SM, Girvin ME: 1H, 13C, 15N backbone NMR assignments of the Staphylococcus aureus small multidrug-resistance pump (Smr) in a functionally active conformation. Biomol NMR Assign 4, 139–142 (2010)

    Girvin ME , '1H, 13C, 15N backbone NMR assignments of the Staphylococcus aureus small multidrug-resistance pump (Smr) in a functionally active conformation ' (2010 ) 4 Biomol NMR Assign : 139 -142 .

    • Search Google Scholar
  • Paulsen IT, Littlejohn TG, Rådström P, Sundström L, Sköld O, Swedberg G, Skurray RA:. The 3’ conserved segment of integrons contains a gene associated with multidrug resistance to antiseptics and disinfectants. Antimicrob Agents Chemother 37, 761–768 (1993)

    Skurray RA , 'The 3’ conserved segment of integrons contains a gene associated with multidrug resistance to antiseptics and disinfectants ' (1993 ) 37 Antimicrob Agents Chemother : 761 -768 .

    • Search Google Scholar
  • Kazama H, Hamashima H, Sasatsu M, Arai T: Distribution of the antiseptic-resistance gene qacE delta 1 in gram-positive bacteria. FEMS Microbiol Lett. 165, 295–299 (1998)

    Arai T , 'Distribution of the antiseptic-resistance gene qacE delta 1 in gram-positive bacteria ' (1998 ) 165 FEMS Microbiol Lett. : 295 -299 .

    • Search Google Scholar
  • Ploy MC, Courvalin P, Lambert T: Characterization of In40 of Enterobacter aerogenes BM2688, a class 1 integron with two new gene cassettes, cmlA2 and qacF. Antimicrob Agents Chemother 42, 2557–2563 (1998)

    Lambert T , 'Characterization of In40 of Enterobacter aerogenes BM2688, a class 1 integron with two new gene cassettes, cmlA2 and qacF ' (1998 ) 42 Antimicrob Agents Chemother : 2557 -2563 .

    • Search Google Scholar
  • Heir E, Sundheim G, Holck AL: The Staphylococcus qacH gene product: a new member of the SMR family encoding multidrug resistance. FEMS Microbiol Lett 163, 49–56 (1998)

    Holck AL , 'The Staphylococcus qacH gene product: a new member of the SMR family encoding multidrug resistance ' (1998 ) 163 FEMS Microbiol Lett : 49 -56 .

    • Search Google Scholar
  • Heir E, Sundheim G, Holck AL: The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. J Appl Microbiol 86, 378–88 (1999)

    Holck AL , 'The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry ' (1999 ) 86 J Appl Microbiol : 378 -88 .

    • Search Google Scholar
  • Bjorland J, Steinum T, Sunde M, Waage S, Heir E: Novel plasmid-borne gene qacJ mediates resistance to quaternary ammonium compounds in equine Staphylococcus aureus, Staphylococcus simulans, and Staphylococcus intermedius. Antimicrob Agents Chemother 47, 3046–3052 (2003)

    Heir E , 'Novel plasmid-borne gene qacJ mediates resistance to quaternary ammonium compounds in equine Staphylococcus aureus, Staphylococcus simulans, and Staphylococcus intermedius ' (2003 ) 47 Antimicrob Agents Chemother : 3046 -3052 .

    • Search Google Scholar
  • Braga TM, Marujo PE, Pomba C, Lopes MFS: Involvement, and dissemination, of the enterococcal small multidrug resistance transporter QacZ in resistance to quaternary ammonium compounds. J Antimicrob Chemother 66, 283–286 (2011)

    Lopes MFS , 'Involvement, and dissemination, of the enterococcal small multidrug resistance transporter QacZ in resistance to quaternary ammonium compounds ' (2011 ) 66 J Antimicrob Chemother : 283 -286 .

    • Search Google Scholar
  • Noguchi N, Suwa J, Narui K, Sasatsu M, Ito T, Hiramatsu K, Song JH: Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999. J Med Microbiol 54, 557–565 (2005)

    Song JH , 'Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999 ' (2005 ) 54 J Med Microbiol : 557 -565 .

    • Search Google Scholar
  • Mayer S, Boos M, Beyer A, Fluit AC, Schmitz FJ: Distribution of the antiseptic resistance genes qacA, qacB and qacC in 497 methicillin-resistant and-susceptible European isolates of Staphylococcus aureus. J Antimicrob Chemother 47, 896–897 (2001)

    Schmitz FJ , 'Distribution of the antiseptic resistance genes qacA, qacB and qacC in 497 methicillin-resistant and-susceptible European isolates of Staphylococcus aureus ' (2001 ) 47 J Antimicrob Chemother : 896 -897 .

    • Search Google Scholar
  • Bjorland J, Steinum T, Kvitle B, Waage S, Sunde M, Heir E: Widespread distribution of disinfectant resistance genes among Staphylococci of bovine and caprine origin in Norway. J Clin Microbiol 43, 4363–4368 (2005)

    Heir E , 'Widespread distribution of disinfectant resistance genes among Staphylococci of bovine and caprine origin in Norway ' (2005 ) 43 J Clin Microbiol : 4363 -4368 .

    • Search Google Scholar
  • Alam MM, Kobayashi N, Uehara N, Watanabe N: Analysis on distribution and genomic diversity of high-level antiseptic resistance genes qacA and qacB in human clinical isolates of Staphylococcus aureus. Microb Drug Resist 9, 109–121 (2003)

    Watanabe N , 'Analysis on distribution and genomic diversity of high-level antiseptic resistance genes qacA and qacB in human clinical isolates of Staphylococcus aureus ' (2003 ) 9 Microb Drug Resist : 109 -121 .

    • Search Google Scholar
  • Shamsudin MN, Alreshidi MA, Hamat RA, Alshrari AS, Atshan SS, Neela V: High prevalence of qacA/B carriage among clinical isolates of meticillin-resistant Staphylococcus aureus in Malaysia. J Hosp Infect 81, 206–208 (2012)

    Neela V , 'High prevalence of qacA/B carriage among clinical isolates of meticillin-resistant Staphylococcus aureus in Malaysia ' (2012 ) 81 J Hosp Infect : 206 -208 .

    • Search Google Scholar
  • Longtin J, Seah C, Siebert K, McGeer A, Simor A, Longtin Y, Low DE, Melano RG: Distribution of antiseptic resistance genes qacA, qacB, and smr in methicillin-resistant Staphylococcus aureus isolated in Toronto, Canada, from 2005 to 2009. Antimicrob Agents Chemother 55, 2999–3001 (2011)

    Melano RG , 'Distribution of antiseptic resistance genes qacA, qacB, and smr in methicillin-resistant Staphylococcus aureus isolated in Toronto, Canada, from 2005 to 2009 ' (2011 ) 55 Antimicrob Agents Chemother : 2999 -3001 .

    • Search Google Scholar
  • McDanel JS, Murphy CR, Diekema DJ, Quan V, Kim DS, Peterson EM, Evans KD, Tan GL, Hayden MK, Huang SS: Chlorhexidine and mupirocin susceptibilities of methicillin-resistant Staphylococcus aureus from colonized nursing home residents. Antimicrob Agents Chemother 57, 552–558 (2013)

    Huang SS , 'Chlorhexidine and mupirocin susceptibilities of methicillin-resistant Staphylococcus aureus from colonized nursing home residents ' (2013 ) 57 Antimicrob Agents Chemother : 552 -558 .

    • Search Google Scholar
  • Mc Gann P, Milillo M, Kwak YI, Quintero R, Waterman PE, Lesho E: Rapid and simultaneous detection of the chlorhexidine and mupirocin resistance genes qacA/B and mupA in clinical isolates of methicillin-resistant Staphylococcus aureus. Diagn Microbiol Infect Dis 77, 270–272 (2013)

    Lesho E , 'Rapid and simultaneous detection of the chlorhexidine and mupirocin resistance genes qacA/B and mupA in clinical isolates of methicillin-resistant Staphylococcus aureus ' (2013 ) 77 Diagn Microbiol Infect Dis : 270 -272 .

    • Search Google Scholar
  • Kosmidis C, Schindler BD, Jacinto PL, Patel D, Bains K, Seo SM, Kaatz GW: Expression of multidrug resistance efflux pump genes in clinical and environmental isolates of Staphylococcus aureus. Int J Antimicrob Agents 40, 204–209 (2012)

    Kaatz GW , 'Expression of multidrug resistance efflux pump genes in clinical and environmental isolates of Staphylococcus aureus ' (2012 ) 40 Int J Antimicrob Agents : 204 -209 .

    • Search Google Scholar
  • Skovgaard S, Larsen MH, Nielsen LN, Skov RL, Wong C, Westh H, Ingmer H: Recently introduced qacA/B genes in Staphylococcus epidermidis do not increase chlorhexidine MIC/MBC. J Antimicrob Chemother 68, 2226–2233 (2013)

    Ingmer H , 'Recently introduced qacA/B genes in Staphylococcus epidermidis do not increase chlorhexidine MIC/MBC ' (2013 ) 68 J Antimicrob Chemother : 2226 -2233 .

    • Search Google Scholar
  • Correa JE, De Paulis A, Predari S, Sordelli DO, Jeric PE: First report of qacG, qacH and qacJ genes in Staphylococcus haemolyticus human clinical isolates. J Antimicrob. Chemother 62, 956–960 (2008)

    Jeric PE , 'First report of qacG, qacH and qacJ genes in Staphylococcus haemolyticus human clinical isolates ' (2008 ) 62 J Antimicrob. Chemother : 956 -960 .

    • Search Google Scholar
  • Prag G, Falk-Brynhildsen K, Jacobsson S, Hellmark B, Unemo M, Söderquist B. Decreased susceptibility to chlorhexidine and prevalence of disinfectant resistance genes among clinical isolates of Staphylococcus epidermidis. APMIS 122, 961–967 (2014)

    Söderquist B , 'Decreased susceptibility to chlorhexidine and prevalence of disinfectant resistance genes among clinical isolates of Staphylococcus epidermidis ' (2014 ) 122 APMIS : 961 -967 .

    • Search Google Scholar
  • Zhang M, O’Dononghue M, Boost M V: Characterization of staphylococci contaminating automated teller machines in Hong Kong. Epidemiol Infect 140, 1366–1371 (2012)

    Boost M V , 'Characterization of staphylococci contaminating automated teller machines in Hong Kong ' (2012 ) 140 Epidemiol Infect : 1366 -1371 .

    • Search Google Scholar
  • Zhou F, Wang Y: Characteristics of antibiotic resistance of airborne Staphylococcus isolated from metro stations. Int J Environ Res Public Health 10, 2412–2426 (2013)

    Wang Y , 'Characteristics of antibiotic resistance of airborne Staphylococcus isolated from metro stations ' (2013 ) 10 Int J Environ Res Public Health : 2412 -2426 .

    • Search Google Scholar
  • Wong TZ, Zhang M, O’Donoghue M, Boost M: Presence of antiseptic resistance genes in porcine methicillin-resistant Staphylococcus aureus. Vet Microbiol 162, 977–979 (2013)

    Boost M , 'Presence of antiseptic resistance genes in porcine methicillin-resistant Staphylococcus aureus ' (2013 ) 162 Vet Microbiol : 977 -979 .

    • Search Google Scholar
  • Heir E, Sundheim G, Holck AL: Identification and characterization of quaternary ammonium compound resistant staphylococci from the food industry. Int J Food Microbiol 48, 211–219 (1999)

    Holck AL , 'Identification and characterization of quaternary ammonium compound resistant staphylococci from the food industry ' (1999 ) 48 Int J Food Microbiol : 211 -219 .

    • Search Google Scholar
  • Wu J, Hassan KA, Skurray RA, Brown MH: Functional analyses reveal an important role for tyrosine residues in the staphylococcal multidrug efflux protein QacA. BMC Microbiol 8, 147 (2008)

    Brown MH , 'Functional analyses reveal an important role for tyrosine residues in the staphylococcal multidrug efflux protein QacA ' (2008 ) 8 BMC Microbiol : 147 -.

    • Search Google Scholar
  • Xu Z, O’Rourke BA, Skurray RA, Brown MH: Role of transmembrane segment 10 in efflux mediated by the staphylococcal multidrug transport protein QacA. J Biol Chem 281, 792–799 (2006)

    Brown MH , 'Role of transmembrane segment 10 in efflux mediated by the staphylococcal multidrug transport protein QacA ' (2006 ) 281 J Biol Chem : 792 -799 .

    • Search Google Scholar
  • Hassan KA, Galea M, Wu J, Mitchell BA, Skurray RA, Brown MH: Functional effects of intramembranous proline substitutions in the staphylococcal multidrug transporter QacA. FEMS Microbiol. Lett 263, 76–85 (2006)

    Brown MH , 'Functional effects of intramembranous proline substitutions in the staphylococcal multidrug transporter QacA ' (2006 ) 263 FEMS Microbiol. Lett : 76 -85 .

    • Search Google Scholar
  • Hassan KA, Skurray RA, Brown MH: Transmembrane helix 12 of the Staphylococcus aureus multidrug transporter QacA lines the bivalent cationic drug binding pocket. J Bacteriol 189, 9131–9134 (2007)

    Brown MH , 'Transmembrane helix 12 of the Staphylococcus aureus multidrug transporter QacA lines the bivalent cationic drug binding pocket ' (2007 ) 189 J Bacteriol : 9131 -9134 .

    • Search Google Scholar
  • Hassan KA, Souhani T, Skurray RA, Brown MH: Analysis of tryptophan residues in the staphylococcal multidrug transporter QacA reveals long-distance functional associations of residues on opposite sides of the membrane. J Bacteriol. 190, 2441–2449 (2008)

    Brown MH , 'Analysis of tryptophan residues in the staphylococcal multidrug transporter QacA reveals long-distance functional associations of residues on opposite sides of the membrane ' (2008 ) 190 J Bacteriol. : 2441 -2449 .

    • Search Google Scholar
  • Paulsen IT, Brown MH, Skurray RA: Characterization of the earliest known Staphylococcus aureus plasmid encoding a multidrug efflux system. J Bacteriol 180, 3477–3479 (1998)

    Skurray RA , 'Characterization of the earliest known Staphylococcus aureus plasmid encoding a multidrug efflux system ' (1998 ) 180 J Bacteriol : 3477 -3479 .

    • Search Google Scholar
  • Sidhu MS, Heir E, Sørum H, Holck A: Genetic linkage between resistance to quaternary ammonium compounds and beta-lactam antibiotics in food-related Staphylococcus spp. Microb Drug Resist 7, 363–371 (2001)

    Holck A , 'Genetic linkage between resistance to quaternary ammonium compounds and beta-lactam antibiotics in food-related Staphylococcus spp ' (2001 ) 7 Microb Drug Resist : 363 -371 .

    • Search Google Scholar
  • Bischoff M, Bauer J, Preikschat P, Schwaiger K, Mölle G, Hölzel C: First detection of the antiseptic resistance gene qacA/B in Enterococcus faecalis. Microb Drug Resist 18, 7–12 (2012)

    Hölzel C , 'First detection of the antiseptic resistance gene qacA/B in Enterococcus faecalis ' (2012 ) 18 Microb Drug Resist : 7 -12 .

    • Search Google Scholar
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Senior editors

Editor(s)-in-Chief: Dunay, Ildiko Rita, Prof. Dr. Pharm, Dr. rer. nat., University of Magdeburg, Germany

Editor(s)-in-Chief: Heimesaat, Markus M., Prof. Dr. med., Charité - University Medicine Berlin, Germany

Editorial Board

  • Berit Bangoura, Dr. DVM. PhD,  University of Wyoming, USA
  • Stefan Bereswill, Prof. Dr. rer. nat., Charité - University Medicine Berlin, Germany
  • Dunja Bruder, Prof. Dr. rer. nat., University of Magdeburg, Germany
  • Jan Buer, Prof. Dr. med., University of Duisburg, Germany
  • Edit Buzas, Prof. Dr. med., Semmelweis University, Hungary
  • Renato Damatta, Prof. PhD, UENF, Brazil
  • Maria Deli, MD, PhD, DSc, Biological Research Center, HAS, Hungary
  • Olgica Djurković-Djaković, Prof. Phd, University of Belgrade, Serbia
  • Jean-Dennis Docquier, Prof. Dr. med., University of Siena, Italy
  • Zsuzsanna Fabry, Prof. Phd, University of Washington, USA
  • Ralf Ignatius, Prof. Dr. med., Charité - University Medicine Berlin, Germany
  • Achim Kaasch, Prof. Dr. med., Otto von Guericke University Magdeburg, Germany
  • Oliver Liesenfeld, Prof. Dr. med., Inflammatix, USA
  • Matyas Sandor, Prof. PhD, University of Wisconsin, USA
  • Ulrich Steinhoff, Prof. PhD, University of Marburg, Germany
  • Michal Toborek, Prof. PhD, University of Miami, USA
  • Susanne A. Wolf, PhD, MDC-Berlin, Germany

 

Dr. Dunay, Ildiko Rita
Magdeburg, Germany
E-mail: ildiko.dunay@med.ovgu.de

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Microbiology (Q3)
Immunology and Allergy (Q3)
Immunology (Q3)
Scopus  
Scopus
Cite Score
5.0
Scopus
CIte Score Rank
Microbiology (medical) Q2
Scopus
SNIP
0.832

 

European Journal of Microbiology and Immunology
Publication Model Gold Open Access
Online only
Submission Fee none
Article Processing Charge 600 EUR/article
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription Information Gold Open Access
Purchase per Title  

European Journal of Microbiology and Immunology
Language English
Size A4
Year of
Foundation
2011
Volumes
per Year
1
Issues
per Year
4
Founder Akadémiai Kiadó
Founder's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 2062-509X (Print)
ISSN 2062-8633 (Online)

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