دورية أكاديمية

Investigation on biofilm composition and virulence traits of S. pseudintermedius isolated from infected and colonized dogs.

التفاصيل البيبلوغرافية
العنوان: Investigation on biofilm composition and virulence traits of S. pseudintermedius isolated from infected and colonized dogs.
المؤلفون: Teixeira IM; Laboratório de Biologia de Anaeróbios, Depto. Microbiologia Médica, IMPPG, UFRJ, Rio de Janeiro, Brazil.; Laboratório de Cocos Gram Positivos, Depto. de Microbiologia e Parasitologia, UFF, Rio de Janeiro, Brazil., de Moraes Assumpção Y; Laboratório de Cocos Gram Positivos, Depto. de Microbiologia e Parasitologia, UFF, Rio de Janeiro, Brazil., Paletta ACC; Laboratório de Cocos Gram Positivos, Depto. de Microbiologia e Parasitologia, UFF, Rio de Janeiro, Brazil., Antunes M; Laboratório de Biologia de Anaeróbios, Depto. Microbiologia Médica, IMPPG, UFRJ, Rio de Janeiro, Brazil., da Silva IT; Laboratório de Cocos Gram Positivos, Depto. de Microbiologia e Parasitologia, UFF, Rio de Janeiro, Brazil., Jaeger LH; Laboratório de Células-Tronco e Parasitologia Molecular, Depto. de Ciências Farmacêuticas, UFJF, Rio de Janeiro, Brazil., Ferreira RF; Curso de Medicina Veterinária da Universidade de Vassouras - Diagnóstico em medicina veterinária - Vassouras, Rio de Janeiro, Brazil., de Oliveira Ferreira E; Laboratório de Biologia de Anaeróbios, Depto. Microbiologia Médica, IMPPG, UFRJ, Rio de Janeiro, Brazil., de Araújo Penna B; Laboratório de Cocos Gram Positivos, Depto. de Microbiologia e Parasitologia, UFF, Rio de Janeiro, Brazil. bpenna@id.uff.br.
المصدر: Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology] [Braz J Microbiol] 2024 Jul 03. Date of Electronic Publication: 2024 Jul 03.
Publication Model: Ahead of Print
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer International Publishing Country of Publication: Brazil NLM ID: 101095924 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1678-4405 (Electronic) Linking ISSN: 15178382 NLM ISO Abbreviation: Braz J Microbiol Subsets: MEDLINE
أسماء مطبوعة: Publication: 2019- : Switzerland, AG : Springer International Publishing
Original Publication: Rio de Janeiro, RJ, Brasil : Sociedade Brasileira de Microbiologia
مستخلص: Staphylococcus pseudintermedius, which is part of the skin microbiome of dogs, causes a variety of opportunistic infections. These infections may become more difficult to treat due to the formation of biofilm. The capacity of S. pseudintermedius to form biofilm, as well as the associated genes, has not been elucidated. This study evaluated the production and composition of S. pseudintermedius biofilm. Samples were collected from both infected dogs and asymptomatic dogs. Isolates were identified using mass spectrometry and Multiplex-PCR. Biofilm production and composition were assessed using a quantitative microtiter plate assay. The presence of ica operon genes and sps genes was investigated using conventional PCR. The investigation of Agr type and virulence genes was conducted in silico on 24 sequenced samples. All strains could produce strong biofilms, with most of the isolates presenting a polysaccharide biofilm. 63.6% of the isolates carried the complete ica operon (ADBC). All samples showed the presence of the genes spsK, spsA, and spsL, while the distribution of other genes varied. Agr type III was the most prevalent (52.2%). All sequenced samples carried the cytotoxins hlb, luk-S, luk-F, as well as the exfoliative toxins siet and se_int. No isolate displayed other exfoliative toxins. Only LB1733 presented a set of different enterotoxins (sea, seb, sec_canine, seh, sek, sel, and seq). Our findings suggest that S. pseudintermedius is a strong producer of biofilm and carries virulence genes.
(© 2024. The Author(s) under exclusive licence to Sociedade Brasileira de Microbiologia.)
References: Devriese LA, Vancanneyt M, Baele M et al (2005) Staphylococcus pseudintermedius sp. nov., a coagulase-positive species from animals. Int J Syst Evol Microbiol 1569–1573. https://doi.org/10.1099/ijs.0.63413-0.
Dmitrenko OA, Balbutskaya AA, Skvortsov VN (2016) Ecological features, pathogenic properties, and role of Staphylococcus intermedius Group representatives in Animal and Human Infectious Pathology. Molekulyarnaya Genetika Mikrobiologiya i Virusologiya 31:117–124. https://doi.org/10.3103/S0891416816030034. (PMID: 10.3103/S0891416816030034)
Bloom P (2013) Canine superficial bacterial folliculitis: current understanding of its etiology, diagnosis and treatment. Vet J 199:217–222. https://doi.org/10.1016/j.tvjl.2013.11.014. (PMID: 10.1016/j.tvjl.2013.11.01424345778)
Penna B, Mendes W, Rabello R, Lilenbaum W (2013) Carriage of methicillin susceptible and resistant Staphylococcus schleiferi among dog with or without topic infections. Vet Microbiol 162:298–299. https://doi.org/10.1016/j.vetmic.2012.08.022. (PMID: 10.1016/j.vetmic.2012.08.02222989516)
Bannoehr J, Guardabassi L (2012) Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Vet Dermatol 23:1–16. https://doi.org/10.1111/j.1365-3164.2012.01046.x. (PMID: 10.1111/j.1365-3164.2012.01046.x)
Phumthanakorn N, Chanchaithong P, Prapasarakul N (2017) Development of a set of multiplex PCRs for detection of genes encoding cell wall-associated proteins in Staphylococcus pseudintermedius isolates from dogs, humans and the environment. J Microbiol Methods 142:90–95. https://doi.org/10.1016/j.mimet.2017.09.003. (PMID: 10.1016/j.mimet.2017.09.00328888869)
Ben Zakour NL, Beatson SA, van den Broek AHM et al (2012) Comparative genomics of the Staphylococcus intermedius group of animal pathogens. Front Cell Infect Microbiol 2:44. https://doi.org/10.3389/fcimb.2012.00044. (PMID: 10.3389/fcimb.2012.00044229196353417630)
Pietrocola G, Gianotti V, Richards AC et al (2015) Fibronectin binding proteins SpsD and SpsL both support invasion of canine epithelial cells by Staphylococcus pseudintermedius. Infect Immun 83:4093–4102. https://doi.org/10.1128/IAI.00542-15. (PMID: 10.1128/IAI.00542-15262387104567651)
Pickering AC, Vitry P, Prystopiuk V et al (2019) Host-specialized fibrinogen-binding by a bacterial surface protein promotes biofilm formation and innate immune evasion. PLoS Pathog 15:1–24. https://doi.org/10.1371/journal.ppat.1007816. (PMID: 10.1371/journal.ppat.1007816)
Singh A, Walker M, Rousseau J, Weese JS (2013) Characterization of the biofilm forming ability of Staphylococcus pseudintermedius from dogs. BMC Vet Res 9:93. https://doi.org/10.1186/1746-6148-9-93. (PMID: 10.1186/1746-6148-9-93236417553681638)
Singh A, Walker M, Rousseau J, Weese JS (2013) Characterization of the biofilm forming ability of S taphylococcus pseudintermedius from dogs.
Stefanetti V, Bietta A, Pascucci L et al (2017) Investigation of the antibiotic resistance and biofilm formation of Staphylococcus pseudintermedius strains isolated from canine pyoderma. Vet Ital 53:289–296. https://doi.org/10.12834/VetIt.465.2275.6. (PMID: 10.12834/VetIt.465.2275.629307122)
Pompilio A, De Nicola S, Crocetta V et al (2015) New insights in Staphylococcus pseudintermedius pathogenicity: antibiotic-resistant biofilm formation by a human wound-associated strain. BMC Microbiol 15:109. https://doi.org/10.1186/s12866-015-0449-x. (PMID: 10.1186/s12866-015-0449-x259944064440327)
Osland AM, Vestby LK, Fanuelsen H et al (2012) Clonal diversity and biofilm-forming ability of methicillin-resistant Staphylococcus pseudintermedius. J Antimicrob Chemother 67:841–848. https://doi.org/10.1093/jac/dkr576. (PMID: 10.1093/jac/dkr57622258925)
Wolska KI, Grudniak AM, Rudnicka Z, Markowska K (2016) Genetic control of bacterial biofilms. J Appl Genet 57:225–238. https://doi.org/10.1007/s13353-015-0309-2. (PMID: 10.1007/s13353-015-0309-226294280)
Otto M (2018) Staphylococcal biofilms. Microbiol Spectr 6:1–17. https://doi.org/10.1128/microbiolspec.GPP3-0023-2018.Correspondence. (PMID: 10.1128/microbiolspec.GPP3-0023-2018.Correspondence)
Arciola CR, Gamberini S, Campoccia D et al (2005) A multiplex PCR method for the detection of all five individual genes of ica locus in Staphylococcus epidermidis. A survey on 400 clinical isolates from prosthesis-associated infections. J Biomed Mater Res 75:408–413. https://doi.org/10.1002/jbm.a.30445. (PMID: 10.1002/jbm.a.30445)
Arciola CR, Campoccia D (2018) Implant infections: adhesion, biofilm formation and immune evasion. Nat Rev Microbiol 16:397–409. https://doi.org/10.1038/s41579-018-0019-y. (PMID: 10.1038/s41579-018-0019-y29720707)
Little SV, Bryan LK, Hillhouse AE et al (2019) Characterization of agr groups of Staphylococcus pseudintermedius isolates from dogs in Texas. mSphere 4:1–11. https://doi.org/10.1128/msphere.00033-19. (PMID: 10.1128/msphere.00033-19)
Kang M, Chae M, Yoon J et al (2014) Antibiotic resistance and molecular characterization of ophthalmic Staphylococcus pseudintermedius isolates from dogs. Veterinary Sci 15:409–415. (PMID: 10.4142/jvs.2014.15.3.409)
Perreten V, Finn M, Greko C et al (2010) Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. J Antimicrob Chemother 65:1–10. https://doi.org/10.1093/jac/dkq078. (PMID: 10.1093/jac/dkq078)
Carroll KC, Burnham CAD, Westblade LF (2021) From canines to humans: clinical importance of Staphylococcus pseudintermedius. PLoS Pathog 17. https://doi.org/10.1371/journal.ppat.1009961.
Lozano C, Rezusta A, Ferrer I et al (2017) Staphylococcus pseudintermedius Human infection cases in Spain: dog-to-human transmission. Vector-Borne Zoonotic Dis 17. https://doi.org/10.1089/vbz.2016.2048 .:vbz.2016.2048.
Somayaji R, Priyantha MAR, Rubin JE, Church D (2016) Human infections due to Staphylococcus pseudintermedius, an emerging zoonosis of canine origin: report of 24 cases. Diagn Microbiol Infect Dis 85:471–476. https://doi.org/10.1016/j.diagmicrobio.2016.05.008. (PMID: 10.1016/j.diagmicrobio.2016.05.00827241371)
Riegel P, Jesel-morel L, Laventie B et al (2011) Coagulase-positive Staphylococcus pseudintermedius from animals causing human endocarditis. Int J Med Microbiol 301:237–239. https://doi.org/10.1016/j.ijmm.2010.09.001. (PMID: 10.1016/j.ijmm.2010.09.00121075051)
Stegmann R, Burnens A, Maranta CA, Perreten V (2010) Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71.
Hoovels L, Van, Vankeerberghen A, Boel A et al (2006) First Case of Staphylococcus pseudintermedius infection in a human. J Clin Microbiol 44:4609–4612. https://doi.org/10.1128/JCM.01308-06. (PMID: 10.1128/JCM.01308-06170508171698428)
Bhooshan S, Negi V, Khatri PK (2020) Staphylococcus pseudintermedius: an undocumented, emerging pathogen in humans. GMS Hyg Infect Control 15:1–11.
Stepanovic S, Vukovic D, Hola V et al (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Acta Pathologica Microbiol et Immunol Scand 115:891–899. https://doi.org/10.1111/j.1600-0463.2007.apm_630.x. (PMID: 10.1111/j.1600-0463.2007.apm_630.x)
Sasaki T, Tsubakishita S, Tanaka Y et al (2010) Multiplex-PCR method for species identification of coagulase-positive staphylococci. J Clin Microbiol 48:765–769. https://doi.org/10.1128/JCM.01232-09. (PMID: 10.1128/JCM.01232-09200538552832457)
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-Based typing from forensic material. Biotechniques 10:506–513. (PMID: 1867860)
Côrtes MF, Beltrame CO, Ramundo MS et al (2015) International Journal of Medical Microbiology the influence of different factors including fnbA and mecA expression on biofilm formed by MRSA clinical isolates with different genetic backgrounds. Int J Med Microbiol 305:140–147. https://doi.org/10.1016/j.ijmm.2014.11.011. (PMID: 10.1016/j.ijmm.2014.11.01125547264)
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. 75:4728–4742. https://doi.org/10.1128/IAI.00640-07.
Zhang K, Mcclure J, Louie T, Conly JM (2005) Novel multiplex PCR assay for characterization and concomitant subtyping of Staphylococcal Cassette chromosome. Microbiol (N Y) 43:5026–5033. https://doi.org/10.1128/JCM.43.10.5026. (PMID: 10.1128/JCM.43.10.5026)
Proietti PC, Stefanetti V, Hyatt DR et al (2015) Phenotypic and genotypic characterization of canine pyoderma isolates of Staphylococcus pseudintermedius for biofilm formation. J Vet Med Sci/Jpn Soc Vet Sci 77:945–951. https://doi.org/10.1292/jvms.15-0043. (PMID: 10.1292/jvms.15-0043)
Meroni G, Filipe JFS, Drago L, Martino PA (2019) Investigation on antibiotic-resistance, biofilm formation and virulence factors in multi drug resistant and non multi drug resistant Staphylococcus pseudintermedius. Microorganisms 7. https://doi.org/10.3390/microorganisms7120702.
Han J-I, Yang C-H, Park H-M (2015) Emergence of biofilm-producing Staphylococcus pseudintermedius isolated from healthy dogs in South Korea. Veterinary Q 2176:1–11. https://doi.org/10.1080/01652176.2015.1096429. (PMID: 10.1080/01652176.2015.1096429)
Walker M, Singh A, Nazarali A et al (2016) Evaluation of the impact of Methicillin-Resistant Staphylococcus pseudintermedius Biofilm formation on Antimicrobial susceptibility. Vet Surg 45:968–971. https://doi.org/10.1111/vsu.12535. (PMID: 10.1111/vsu.1253527500604)
Gara JPO (2007) Ica and beyond: bio ¢ lm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. 270:179–188. https://doi.org/10.1111/j.1574-6968.2007.00688.x.
Filho RGS, Lima AA, Saramago CSM et al (2015) Biofilm production by clinical isolates of Staphylococcus epidermidis and its relationship with genotypic profile, presence of virulence-related genes and antibiotic resistance. Afr J Microbiol Res 9:1026–1036. https://doi.org/10.5897/AJMR2014.6835. (PMID: 10.5897/AJMR2014.6835)
Arima S, Ochi H, Mitsuhashi M et al (2018) Staphylococcus pseudintermedius biofilms secrete factors that induce inflammatory reactions in vitro. Lett Appl Microbiol 67:214–219. https://doi.org/10.1111/lam.13018. (PMID: 10.1111/lam.1301829893497)
Figueiredo AMS, Ferreira FA, Beltrame CO, Côrtes MF (2017) The role of biofilms in persistent infections and factors involved in ica-independent biofilm development and gene regulation in Staphylococcus aureus Staphylococcus aureus. Crit Rev Microbiol 43:602–620. https://doi.org/10.1080/1040841X.2017.1282941. (PMID: 10.1080/1040841X.2017.128294128581360)
Bannoehr J, Brown JK, Shaw DJ et al (2011) Staphylococccus Pseudintermedius surface proteins SpsD and SpsO mediate adherence to ex vivo canine corneocytes. Vet Dermatol 23:119–125. https://doi.org/10.1111/j.1365-3164.2011.01021.x. (PMID: 10.1111/j.1365-3164.2011.01021.x22112246)
Bannoehr J, Zakour NLB, Reglinski M et al (2011) Genomic and surface proteomic analysis of the canine pathogen Staphylococcus pseudintermedius reveals proteins that mediate adherence to the extracellular matrix. Infect Immun 79:3074–3086. https://doi.org/10.1128/IAI.00137-11. (PMID: 10.1128/IAI.00137-11215763333147560)
Richards AC, O’Shea M, Beard PM et al (2018) Staphylococcus pseudintermedius surface protein L (SpsL) is required for abscess formation in a murine cutaneous infection model. https://doi.org/10.1128/IAI.00631-18 . Infect Immun.
Zukancic A, Khan MA, Gurmen SJ et al (2020) Staphylococcal protein A (spa) locus is a hot spot for recombination and Horizontal Gene Transfer in Staphylococcus pseudintermedius. https://doi.org/10.1128/msphere.00666-20 . mSphere 5:.
Grandolfo E (2018) Looking through Staphylococcus pseudintermedius infections: could spa be considered a possible vaccine target? Virulence 9:703–706. https://doi.org/10.1080/21505594.2018.1426964. (PMID: 10.1080/21505594.2018.1426964294579885955435)
Couto N, Belas A, Oliveira M et al (2015) Comparative analysis of the virulence characteristics of methicillin–resistant and – susceptible Staphylococcus pseudintermedius isolates isolated from small animals: a RNA-Seq-based transcriptome analysis. Antimicrob Agents Chemother 60:962–967. https://doi.org/10.1128/AAC.01907-15. (PMID: 10.1128/AAC.01907-1526621622)
Couto N, Martins J, Mafalda A et al (2015) Identi fi cation of vaccine candidate antigens of Staphylococcus pseudintermedius by whole proteome characterization and serological proteomic analyses. J Proteom. https://doi.org/10.1016/j.jprot.2015.12.017. (PMID: 10.1016/j.jprot.2015.12.017)
معلومات مُعتمدة: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; Conselho Nacional de Desenvolvimento Científico e Tecnológico Conselho Nacional de Desenvolvimento Científico e Tecnológico; Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro; Bill and Melinda Gates Foundation Bill and Melinda Gates Foundation
فهرسة مساهمة: Keywords: Staphylococcus pseudintermedius; biofilm; Surface proteins; Virulence factors
تواريخ الأحداث: Date Created: 20240702 Latest Revision: 20240702
رمز التحديث: 20240703
DOI: 10.1007/s42770-024-01405-y
PMID: 38955982
قاعدة البيانات: MEDLINE
الوصف
تدمد:1678-4405
DOI:10.1007/s42770-024-01405-y