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Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 36, 2020 - Issue 1
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Original Articles

Various biofilm matrices of the emerging pathogen Staphylococcus lugdunensis: exopolysaccharides, proteins, eDNA and their correlation with biofilm mass

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Pages 86-100 | Received 30 Jun 2019, Accepted 10 Jan 2020, Published online: 27 Jan 2020

References

  • Arciola CR, Campoccia D, Montanaro L. 2018. Implant infections: adhesion, biofilm formation and immune evasion. Nat Rev Microbiol. 16:397–409. doi:10.1038/s41579-018-0019-y
  • Arciola CR, Campoccia D, Ravaioli S, Montanaro L. 2015. Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects. Front Cell Infect Microbiol. 5:7.
  • Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW. 2012. Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials. 33:5967–5982. doi:10.1016/j.biomaterials.2012.05.031
  • Arciola CR, Caramazza R, Pizzoferrato A. 1994. In vitro adhesion of Staphylococcus epidermidis on heparin-surface-modified intraocular lenses. J Cataract Refract Surg. 20:158–161. doi:10.1016/S0886-3350(13)80157-5
  • Arciola CR, Montanaro L, Moroni A, Giordano M, Pizzoferrato A, Donati ME. 1999. Hydroxyapatite-coated orthopaedic screws as infection resistant materials: in vitro study. Biomaterials. 20:323–327. doi:10.1016/S0142-9612(98)00168-9
  • Arciola CR, Radin L, Alvergna P, Cenni E, Pizzoferrato A. 1993. Heparin surface treatment of poly(methylmethacrylate) alters adhesion of a Staphylococcus aureus strain: utility of bacterial fatty acid analysis. Biomaterials. 14:1161–1164. doi:10.1016/0142-9612(93)90161-T
  • Argemi X, Hansmann Y, Riegel P, Prévost G. 2017. Is Staphylococcus lugdunensis significant in clinical samples? J Clin Microbiol. 55(11):3167–3174. doi:10.1128/JCM.00846-17
  • Argemi X, Hansmann Y, Prola K, Prévost G. 2019. Coagulase-negative staphylococci pathogenomics. Int J Mol Sci. 20(5). pii: E1215.
  • Campoccia D, Mirzaei R, Montanaro L, Arciola CR. 2019. Hijacking of immune defences by biofilms: a multifront strategy. Biofouling. 35:1055–1074. doi:10.1080/08927014.2019.1689964
  • Campoccia D, Montanaro L, Ravaioli S, Pirini V, Cangini I, Arciola C.R. 2011. Exopolysaccharide production by Staphylococcus epidermidis and its relationship with biofilm extracellular DNA. Int J Artif Organs. 34:832–839. doi:10.5301/ijao.5000048
  • Cheng CW, Liu TP, Yeh CF, Lee MH, Chang SC, Lu JJ. 2015. Persistence of a major endemic clone of oxacillin-resistant Staphylococcus lugdunensis sequence type 6 at a tertiary medical centre in northern Taiwan. Int J Infect Dis. 36:72–77. doi:10.1016/j.ijid.2015.05.022
  • Frank KL, Del Pozo JL, Patel R. 2008. From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev. 21:111–133. doi:10.1128/CMR.00036-07
  • Dubois-Brissonnet F, Trotier E, Briandet R. 2016. The biofilm lifestyle involves an increase in bacterial membrane saturated fatty acids. Front Microbiol. 28:1673.
  • Ebright JR, Penugonda N, Brown W. 2004. Clinical experience with Staphylococcus lugdunensis bacteremia: a retrospective analysis. Diagn Microbiol Infect Dis. 48:17–21. doi:10.1016/j.diagmicrobio.2003.08.008
  • Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. 2016. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 14:563–575. doi:10.1038/nrmicro.2016.94
  • Frank KL, Patel R. 2007. Poly-N-acetylglucosamine is not a major component of the extracellular matrix in biofilms formed by icaADBC-positive Staphylococcus lugdunensis isolates. Infect Immun. 75:4728–4742. doi:10.1128/IAI.00640-07
  • Frank KL, Reichert EJ, Piper KE, Patel R. 2007. In vitro effects of antimicrobial agents on planktonic and biofilm forms of Staphylococcus lugdunensis clinical isolates. Antimicrob Agents Chemother. 51:888–895. doi:10.1128/AAC.01052-06
  • Freney J, Brun Y, Bes M, Meugnier H, Grimont F, Grimont P, Nervi C, Fleurette J. 1988. Staphylococcus lugdunensis sp. nov and Staphylococcus schleiferi sp. nov., two species from human clinical specimens. Int J Syst Evol Microbiol. 38:168–172.
  • Gibert L, Didi J, Marlinghaus L, Lesouhaitier O, Legris S, Szabados F, Pons JL, Pestel-Caron M. 2014. The major autolysin of Staphylococcus lugdunensis, AtlL, is involved in cell separation, stress-induced autolysis and contributes to bacterial pathogenesis. FEMS Microbiol Lett. 352:78–86. doi:10.1111/1574-6968.12374
  • Giormezis N, Kolonitsiou F, Makri A, Vogiatzi A, Christofidou M, Anastassiou ED, Spiliopoulou I. 2015. Virulence factors among Staphylococcus lugdunensis are associated with infection sites and clonal spread. Eur J Clin Microbiol Infect Dis. 34:773–778. doi:10.1007/s10096-014-2291-8
  • Hellbacher C, Törnqvist E, Söderquist B. 2006. Staphylococcus lugdunensis: clinical spectrum, antibiotic susceptibility, and phenotypic and genotypic patterns of 39 isolates. Clin Microbiol Infect. 12:43–49. doi:10.1111/j.1469-0691.2005.01296.x
  • Hiltunen AK, Savijoki K, Nyman TA, Miettinen I, Ihalainen P, Peltonen J, Fallarero A. 2019. Structural and functional dynamics of Staphylococcus aureus biofilms and biofilm matrix proteins on different clinical materials. Microorganisms. 7:584. doi:10.3390/microorganisms7120584
  • Ho PL, Leung SM, Chow KH, Tse CW, Cheng VC, Tse H, Mak SK, Lo WK. 2015. Carriage niches and molecular epidemiology of Staphylococcus lugdunensis and methicillin-resistant S. lugdunensis among patients undergoing long-term renal replacement therapy. Diagn Microbiol Infect Dis. 81:141–144. doi:10.1016/j.diagmicrobio.2014.10.004
  • Hussain M, Steinbacher T, Peters G, Heilmann C, Becker K. 2015. The adhesive properties of the Staphylococcus lugdunensis multifunctional autolysin AtlL and its role in biofilm formation and internalization. Int J Med Microbiol. 305:129–139. doi:10.1016/j.ijmm.2014.11.010
  • Ibáñez de Aldecoa AL, Zafra O, González-Pastor JE. 2017. Mechanisms and regulation of extracellular DNA release and its biological roles in microbial communities. Front Microbiol. 8:1390. doi:10.3389/fmicb.2017.01390
  • Joo HS, Otto M. 2012. Molecular basis of in vivo biofilm formation by bacterial pathogens. Chem Biol. 19:1503–1513. doi:10.1016/j.chembiol.2012.10.022
  • Kaplan JB. 2009. Therapeutic potential of biofilm-dispersing enzymes. Int J Artif Organs. 32:545–554. doi:10.1177/039139880903200903
  • Kaplan JB, Mlynek KD, Hettiarachchi H, Alamneh YA, Biggemann L, Zurawski DV, Black CC, Bane CE, Kim RK, Granick MS. 2018. Extracellular polymeric substance (EPS)-degrading enzymes reduce staphylococcal surface attachment and biocide resistance on pig skin in vivo. PLoS One. 13:e0205526. doi:10.1371/journal.pone.0205526
  • Kleiner E, Monk AB, Archer GL, Forbes BA. 2010. Clinical significance of Staphylococcus lugdunensis isolated from routine cultures. Clin Infect Dis. 51:801–803. doi:10.1086/656280
  • Klotchko A, Wallace MR, Licitra C, Sieger B. 2011. Staphylococcus lugdunensis: an emerging pathogen. South Med J. 104:509–514. doi:10.1097/SMJ.0b013e31821e91b1
  • Kogan G, Sadovskaya I, Chaignon P, Chokr A, Jabbouri S. 2006. Biofilms of clinical strains of Staphylococcus that do not contain polysaccharide intercellular adhesin. FEMS Microbiol Lett. 255:11–16. doi:10.1111/j.1574-6968.2005.00043.x
  • Krumperman PH. 1983. Multiple antibiotic resistance indexing Escherichia coli to identify risk sources of faecal contamination of foods. Appl Environ Microbiol. 46:165–170. doi:10.1128/AEM.46.1.165-170.1983
  • Missineo A, Di Poto A, Geoghegan JA, Rindi S, Heilbronner S, Gianotti V, Arciola CR, Foster TJ, Speziale P, Pietrocola G. 2014. IsdC from Staphylococcus lugdunensis induces biofilm formation under low-iron growth conditions. Infect Immun. 82:2448–2459. doi:10.1128/IAI.01542-14
  • Montanaro L, Poggi A, Visai L, Ravaioli S, Campoccia D, Speziale P, Arciola CR. 2011. Extracellular DNA in biofilms. Int J Artif Organs. 34:824–831. doi:10.5301/ijao.5000051
  • Neu T, Swerhone GD, Lawrence JR. 2001. Assessment of lectin-binding analysis for in situ detection of glycoconjugates in biofilm systems. Microbiology. 147:299–313. doi:10.1099/00221287-147-2-299
  • Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D. 2007. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology. 153:2083–2092. doi:10.1099/mic.0.2007/006031-0
  • Rajendran NB, Eikmeier J, Becker K, Hussain M, Peters G, Heilmann C. 2015. Important contribution of the novel Llcus comEB to extracellular DNA-dependent Staphylococcus lugdunensis biofilm formation. Infect Immun. 83:4682–4692. doi:10.1128/IAI.00775-15
  • Ravaioli S, Selan L, Visai L, Pirini V, Campoccia D, Maso A, Speziale P, Montanaro L, Arciola CR. 2012. Staphylococcus lugdunensis, an aggressive coagulase-negative pathogen not to be underestimated. Int J Artif Organs. 35:742–753. doi:10.5301/ijao.5000142
  • Ravaioli S, Campoccia D, Visai L, Pirini V, Cangini I, Corazzari T, Maso A, Poggio C, Pegreffi F, Montanaro L, et al. 2011. Biofilm extracellular-DNA in 55 Staphylococcus epidermidis clinical isolates from implant infections. Int J Artif Organs. 34:840–846. doi:10.5301/ijao.5000057
  • Sadovskaya I, Chaignon P, Kogan G, Chokr A, Vinogradov E, Jabbouri S. 2006. Carbohydrate-containing components of biofilms produced in vitro by some staphylococcal strains related to orthopaedic prosthesis infections. FEMS Immunol Med Microbiol. 47:75–82. doi:10.1111/j.1574-695X.2006.00068.x
  • Seng P, Traore M, Lavigne JP, Maulin L, Lagier JC, Thiery JF, Levy PY, Roger PM, Bonnet E, Sotto A, et al. 2017. Staphylococcus lugdunensis: a neglected pathogen of infections involving fracture-fixation devices. International Orthopaedics (Sicot)). 41:1085–1091. doi:10.1007/s00264-017-3476-4
  • Seviour T, Derlon N, Dueholm MS, Flemming HC, Girbal-Neuhauser E, Horn H, Kjelleberg S, van Loosdrecht MCM, Lotti T, Malpei MF, et al. 2019. Extracellular polymeric substances of biofilms: Suffering from an identity crisis. Water Res. 151:1–7. doi:10.1016/j.watres.2018.11.020
  • Taha L, Stegger M, Söderquist B. 2019. Staphylococcus lugdunensis: antimicrobial susceptibility and optimal treatment options. Eur J Clin Microbiol Infect Dis. 38:1449–1455. doi:10.1007/s10096-019-03571-6
  • Tseng SP, Lin YT, Tsai JC, Hung WC, Chen HJ, Chen PF, Hsueh PR, Teng LJ. 2015. Genotypes and phenotypes of Staphylococcus lugdunensis isolates recovered from bacteremia. J Microbiol Immunol Infect. 48:397–405. doi:10.1016/j.jmii.2013.11.006
  • Vorkapic D, Pressler K, Schild S. 2016. Multifaceted roles of extracellular DNA in bacterial physiology. Curr Genet. 62:71–79. doi:10.1007/s00294-015-0514-x
  • Wagner M, Ivleva NP, Haisch C, Niessner R, Horn H. 2009. Combined use of confocal laser scanning microscopy (CLSM) and Raman microscopy (RM): investigations on EPS-Matrix. Water Res. 43:63–76. doi:10.1016/j.watres.2008.10.034
  • Yeh CF, Liu TP, Cheng CW, Chang SC, Lee MH, Lu JJ. 2015. Molecular characteristics of disease-causing and commensal Staphylococcus lugdunensis isolates from 2003 to 2013 at a tertiary hospital in Taiwan. PLoS One. 10:e0134859. doi:10.1371/journal.pone.0134859
  • Zatorska B, Arciola CR, Haffner N, Segagni Lusignani L, Presterl E, Diab-Elschahawi M. 2018. Bacterial extracellular DNA production is associated with outcome of prosthetic joint infections. Biomed Res Int. 1067413. 2018:1–6. eCollection 2018. doi:10.1155/2018/1067413

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