Hypervirulent Klebsiella pneumoniae serotype K1 clinical isolates form robust biofilms at the air-liquid interface
Autoři:
Meritxell Cubero aff001; Sara Marti aff001; Mª Ángeles Domínguez aff001; Aida González-Díaz aff001; Dàmaris Berbel aff001; Carmen Ardanuy aff001
Působiště autorů:
Department of Microbiology, Hospital Universitari de Bellvitge, Instituto de Investigación Biomédica de Bellvitge (IDIBELL), Barcelona, Spain
aff001; Research Network for Respiratory Diseases (CIBERES), ISCIII, Madrid, Spain
aff002; Spanish Network for Research in Infectious Diseases (REIPI), Barcelona, Spain
aff003; Departamento de Patología y terapéutica experimental, Universitat de Barcelona, Barcelona, Spain
aff004
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222628
Souhrn
The prevalence of a new hypervirulent and hypermucoviscous K. pneumoniae phenotype (Hmv) is increasing worldwide, mainly linked to serotypes K1 and K2. Since capsular thickness can directly affect the capability to form biofilms, we aimed to evaluate the association between the Hmv phenotype with adhesion and biofilm formation in a collection of clinical K. pneumoniae isolates.
We selected 38 Hmv clinical isolates [15 serotype K1; 9 serotype K2; 3 non-K1/K2 (rmpA+); 11 non-K1/K2 (rmpA-)] and 7 non-Hmv clinical isolates. The Hmv phenotype was assessed through the mucoviscosity test. Serum resistance was determined by bacterial viability tests in pooled human serum. Adhesion was evaluated with the Biofilm Ring Test®, and biofilm formation was identified by crystal violet staining (Solid-Liquid, SLI-biofilm) or visual examination (Air-Liquid, ALI-biofilm).
This study linked for the first time the formation of robust ALI-biofilm plugs by K. pneumoniae to the capsular serotype K1, a group of hypervirulent strains which are generally highly susceptible to the antimicrobial agents. Among all the studied isolates, the capsular serotype K1 presented lower initial adhesion despite having the adhesins mrkD and fimH but higher ALI-biofilm formation than isolates with other capsular serotypes (K2 or non-K1/K2). This structure might confer increased resistance to a group of hypervirulent K. pneumoniae serotype K1.
Klíčová slova:
Biology and life sciences – Cell biology – Organisms – Research and analysis methods – Medicine and health sciences – Cellular structures and organelles – Pili and fimbriae – Microbiology – Medical microbiology – Microbial pathogens – Bacterial pathogens – Bacteria – Pathology and laboratory medicine – Pathogens – Virulence factors – Pathogen motility – Bacteriology – Bacterial physiology – Microbial physiology – Bacterial biofilms – Biofilms – Specimen preparation and treatment – Staining – Klebsiella – Adhesins – Crystal violet staining
Zdroje
1. Kanj S, Kanafani Z. Current Concepts in Antimicrobial Therapy Against Resistant Gram-Negative Organisms: Extended-Spectrum β-Lactamase–Producing Enterobacteriaceae, Carbapenem-Resistant Enterobacteriaceae, and Multidrug-Resistant Pseudomonas aeruginosa. Mayo Clin Proc. 2011;86: 250–259. doi: 10.4065/mcp.2010.0674
2. Podschun R, Ullmann U. Klebsiella spp. as Nosocomial Pathogens: Epidemiology, Taxonomy, Typing Methods, and Pathogenicity Factors. Clin Microbiol Rev. 1998;11: 589–603. Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC88898/pdf/cm000589.pdf 9767057
3. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2: 95–108. doi: 10.1038/nrmicro821 15040259
4. Patel G, Shah N, Sharma R. Pyogenic Liver Abscess, Bacteremia, and Meningitis with Hypermucoviscous Klebsiella pneumoniae: An Unusual Case Report in a Human T-Cell Lymphotropic Virus Positive Patient of Caribbean Origin in the United States. Case Rep Infect Dis. Hindawi Publishing Corporation; 2013;2013: 676340. doi: 10.1155/2013/676340 24490092
5. Cubero M, Grau I, Tubau F, Pallarés R, Dominguez MA, Liñares J, et al. Hypervirulent Klebsiella pneumoniae clones causing bacteraemia in adults in a teaching hospital in Barcelona, Spain (2007–2013). Clin Microbiol Infect. 2016;22: 154–160. doi: 10.1016/j.cmi.2015.09.025
6. Struve C, Roe CC, Stegger M, Stahlhut SG, Hansen DS, Engelthaler DM, et al. Mapping the Evolution of Hypervirulent Klebsiella pneumoniae. MBio. 2015;6: e00630–15. doi: 10.1128/mBio.00630-15 26199326
7. Wu KM, Li NH, Yan JJ, Tsao N, Liao TL, Tsai HC, et al. Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitis. J Bacteriol. 2009;191: 4492–4501. doi: 10.1128/JB.00315-09 19447910
8. Schembri MA, Dalsgaard D, Klemm P. Capsule Shields the Function of Short Bacterial Adhesins. J Bacteriol. 2004;186: 1249–1257. doi: 10.1128/JB.186.5.1249-1257.2004 14973035
9. Struve C, Krogfelt KA. Role of capsule in Klebsiella pneumoniae virulence: lack of correlation between in vitro and in vivo studies. FEMS Microbiol Lett. 2003;218(1): 149–154. Available: www.fems-microbiology.org 12583911
10. Fang CT, Chuang YP, Shun CT, Chang SC, Wang JT. A Novel Virulence Gene in Klebsiella pneumoniae Strains Causing Primary Liver Abscess and Septic Metastatic Complications. J Exp Med. Rockefeller University Press; 2004;199: 697–705. doi: 10.1084/jem.20030857 14993253
11. Wu MC, Lin TL, Hsieh PF, Yang HC, Wang JT. Isolation of Genes Involved in Biofilm Formation of a Klebsiella pneumoniae Strain Causing Pyogenic Liver Abscess. PLoS One. 2011;6: e23500. doi: 10.1371/journal.pone.0023500 21858144
12. Lai Y-C, Peng H-L, Chang H-Y. RmpA2, an Activator of Capsule Biosynthesis in Klebsiella pneumoniae CG43, Regulates K2 cps Gene Expression at the Transcriptional Level. J Bacteriol. 2003;185: 788–800. doi: 10.1128/JB.185.3.788-800.2003 12533454
13. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci. 2015;112: e3574–e3581. doi: 10.1073/pnas.1501049112 26100894
14. Brisse S, Fevre C, Passet V, Issenhuth-Jeanjean S, Gis Tournebize R, Diancourt L, et al. Virulent Clones of Klebsiella pneumoniae: Identification and Evolutionary Scenario Based on Genomic and Phenotypic Characterization. PLoS One. 2009;4: e4982. doi: 10.1371/journal.pone.0004982 19319196
15. Bachman MA, Oyler JE, Burns SH, Caza M, Lépine F, Dozois CM, et al. Klebsiella pneumoniae Yersiniabactin Promotes Respiratory Tract Infection through Evasion of Lipocalin 2. Infect Immun. 2011;79: 3309–3316. doi: 10.1128/IAI.05114-11 21576334
16. Diago-Navarro E, Chen L, Passet V, Burack S, Ulacia-Hernando A, Kodiyanplakkal RP, et al. Carbapenem-Resistant Klebsiella pneumoniae Exhibit Variability in Capsular Polysaccharide and Capsule Associated Virulence Traits. J Infect Dis. 2014;210: 803–813. doi: 10.1093/infdis/jiu157 24634498
17. Puig C, Marti S, Hermans PWM, de Jonge MI, Ardanuy C, Liñares J, et al. Incorporation of phosphorylcholine into the lipooligosaccharide of nontypeable Haemophilus influenzae does not correlate with the level of biofilm formation in vitro. Infect Immun. 2014;82: 1591–1599. doi: 10.1128/IAI.01445-13 24452688
18. Puig C, Domenech A, Garmendia J, Langereis JD, Mayer P, Calatayud L, et al. Increased Biofilm Formation by Nontypeable Haemophilus influenzae Isolates from Patients with Invasive Disease or Otitis Media versus Strains Recovered from Cases of Respiratory Infections. Appl Environ Microbiol. 2014;80: 7088–7095. doi: 10.1128/AEM.02544-14 25192997
19. Chavant P, Gaillard-Martinie B, Talon R, Hébraud M, Bernardi T. A new device for rapid evaluation of biofilm formation potential by bacteria. J Microbiol Methods. 2007;68: 605–612. doi: 10.1016/j.mimet.2006.11.010 17218029
20. Nait Chabane Y, Marti S, Rihouey C, Alexandre S, Hardouin J. Characterisation of Pellicles Formed by Acinetobacter baumannii at the Air-Liquid Interface. PLoS One. 2014;9: e111660. doi: 10.1371/journal.pone.0111660 25360550
21. Shon AS, Bajwa RP, Russo TA. Hypervirulent (hypermucoviscous) Klebsiella pneumoniae: a new and dangerous breed. Virulence. 2013;4: 107–118. doi: 10.4161/viru.22718 23302790
22. Merino S, Camprubi S, Alberti S, Benedi V-J, Tomas JM. Mechanisms of Klebsiella pneumoniae Resistance to Complement-Mediated Killing. Infect Immun. 1992;60: 2529–2535. Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC257192/pdf/iai00030-0395.pdf 1587619
23. June HW, Wu AM, Cheng GT, Chang XY, Tsai SF, Wu TS. Contribution of fucose-containing capsules in Klebsiella pneumoniae to bacterial virulence in mice. Exp Biol Med. 2008;233: 64–70. doi: 10.3181/0706-RM-170 18156307
24. Fang C-T, Lai S-Y, Yi W-C, Hsueh P-R, Liu K-L, Chang S-C. Klebsiella pneumoniae Genotype K1: An Emerging Pathogen That Causes Septic Ocular or Central Nervous System Complications from Pyogenic Liver Abscess. Clin Infect Dis. 2007;45: 284–293. doi: 10.1086/519262 17599305
25. Nassif X, Sansonetti PJ. Correlation of the Virulence of Klebsiella pneumoniae KI and K2 with the Presence of a Plasmid Encoding Aerobactin. Infect Immun. 1986;54: 603–608. Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC260211/pdf/iai00099-0009.pdf
26. Hentzien M, Rosman J, Decré D, Brenkle K, Mendes-Martins L, Mateu P. Seven hypervirulent ST380 Klebsiella pneumoniae septic localizations Sept localisations. Médecine Mal Infect. 2017;47: 171–173. doi: 10.1016/j.medmal.2016.10.002
27. Stahlhut SG, Struve C, Krogfelt KA, Reisner A. Biofilm formation of Klebsiella pneumoniae on urethral catheters requires either type 1 or type 3 fimbriae. FEMS immunol med microbiol. 2012;65: 350–359. doi: 10.1111/j.1574-695X.2012.00965.x 22448614
28. Hall-Stoodley L, Stoodley P. Evolving concepts in biofilm infections. Cell Microbiol. 2009;11: 1034–1043. doi: 10.1111/j.1462-5822.2009.01323.x 19374653
29. Alcántar-Curiel MD, Blackburn D, Saldaña Z, Gayosso-Vázquez C, Iovine N, De La Cruz MA, et al. Multi-functional analysis of Klebsiella pneumoniae fimbrial types in adherence and biofilm formation. Virulence. 2013;129: 129–138. doi: 10.4161/viru.22974 23302788
30. Guo Y, Wang S, Zhan L, Jin Y, Duan J, Hao Z, et al. Microbiological and Clinical Characteristics of Hypermucoviscous Klebsiella pneumoniae Isolates Associated with Invasive Infections in China. Front Cell Infect Microbiol. 2017;7: 24. doi: 10.3389/fcimb.2017.00024 28203549
31. Wang H, Wilksch JJ, Strugnell RA, Gee ML. Role of Capsular Polysaccharides in Biofilm Formation: An AFM Nanomechanics Study. ACS Appl Mater Interfaces. 2015;7: 13007–13013. doi: 10.1021/acsami.5b03041 26034816
32. Armitano J, Méjean V, Jourlin-Castelli C. Gram-negative bacteria can also form pellicles. Environ Microbiol Rep. 2014;6: 534–544. doi: 10.1111/1758-2229.12171 25756106
33. Hadjifrangiskou M, Gu AP, Pinkner JS, Kostakioti M, Zhang EW, Greene SE, et al. Transposon Mutagenesis Identifies Uropathogenic Escherichia coli Biofilm Factors. J Bacteriol. 2012;194: 6195–6205. doi: 10.1128/JB.01012-12 22984258
34. Carabarin-Lima A, León-Izurieta L, Del R, Rocha-Gracia C, Castañeda-Lucio M, Torres C, et al. First evidence of polar flagella in Klebsiella pneumoniae isolated from a patient with neonatal sepsis. J Med Microbiol. 2016;65: 729–737. doi: 10.1099/jmm.0.000291 27283194
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania