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Corynebacterium Diphtheriae Putative Tellurite 662 Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 110(5): 662-668, August 2015 Corynebacterium diphtheriae putative tellurite-resistance protein (CDCE8392_0813) contributes to the intracellular survival in human epithelial cells and lethality of Caenorhabditis elegans Louisy Sanches dos Santos1, Camila Azevedo Antunes2, Cintia Silva dos Santos1, José Augusto Adler Pereira1, Priscila Soares Sabbadini3, Maria das Graças de Luna1, Vasco Azevedo2, Raphael Hirata Júnior1, Andreas Burkovski4, Lídia Maria Buarque de Oliveira Asad5, Ana Luíza Mattos-Guaraldi1/+ 1Universidade do Estado do Rio de Janeiro, Faculdade de Ciências Médicas, Departamento de Microbiologia, Imunologia e Parasitologia, Rio de Janeiro, RJ, Brasil 2Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Departamento de Biologia Geral, Belo Horizonte, MG, Brasil 3Centro Universitário do Maranhão, Centro de Ciências da Saúde, Laboratório de Doenças Bacterianas, São Luís, MA, Brasil 4Friedrich-Alexander-Universität Erlangen-Nürnberg, Lehrstuhl fuer Mikrobiologie, Erlangen, Germany 5Universidade do Estado do Rio de Janeiro, Instituto de Biologia Roberto Alcântara Gomes, Departamento de Biofísica e Biometria, Rio de Janeiro, RJ, Brasil Corynebacterium diphtheriae, the aetiologic agent of diphtheria, also represents a global medical challenge be- 2- cause of the existence of invasive strains as causative agents of systemic infections. Although tellurite (TeO3 ) is toxic 2- 2- to most microorganisms, TeO3 -resistant bacteria, including C. diphtheriae, exist in nature. The presence of TeO3 - resistance (TeR) determinants in pathogenic bacteria might provide selective advantages in the natural environment. In the present study, we investigated the role of the putative TeR determinant (CDCE8392_813 gene) in the virulence at- tributes of diphtheria bacilli. The disruption of CDCE8392_0813 gene expression in the LDCIC-L1 mutant increased 2- susceptibility to TeO3 and reactive oxygen species (hydrogen peroxide), but not to other antimicrobial agents. The LDCIC-L1 mutant also showed a decrease in both the lethality of Caenorhabditis elegans and the survival inside of human epithelial cells compared to wild-type strain. Conversely, the haemagglutinating activity and adherence to and formation of biofilms on different abiotic surfaces were not regulated through the CDCE8392_0813 gene. In conclu- sion, the CDCE8392_813 gene contributes to the TeR and pathogenic potential of C. diphtheriae. Key words: Corynebacterium diphtheriae - tellurite-resistance - CDCE8392_0813 protein - HEp-2 cells - Caenorhabditis elegans Tellurium (Te) is a metalloid that exists as a trace com- Although Te compounds have not been overlooked as ponent in natural environments. Te compounds are used antimicrobial agents, recent investigations studies con- in industrial processes and increased delivery of these cerning their biochemical properties and toxicity mech- compounds into the environment generates pollution in anisms of these molecules have identified Te compounds soil and water, potentially resulting in contamination as potential candidates for use as antibiotics, anticancer and subsequent adverse effects on public health (Avazéri drugs and therapeutic agents for the treatment of Parkin- 2- et al. 1997, Aradská et al. 2013). Tellurite (TeO3 ), one son’s disease (Ba et al. 2010, Sekhon 2013). Currently, 2- of the most oxidised and soluble forms of Te, is toxic to TeO3 is used as a selective agent in the culture media of both prokaryotes and eukaryotes. Among prokaryotes, some pathogens, such as Corynebacterium diphtheriae Gram-negative bacteria are particularly susceptible to and Staphylococcus aureus (Taylor 1999). Te salts, whereas some Gram-positive bacteria are natu- Although little is known about the mechanisms of 2- R rally resistant. Te compounds have a long history as an- TeO3 -resistance (Te ), numerous plasmid and/or chromo- timicrobial and therapeutic agents for the treatment of somally encoded TeR determinants have been identified infectious diseases, e.g., hanseniasis and tuberculosis. in different bacterial species, including human pathogens. The presence of TeR determinants in pathogenic bacteria suggests that these genes might provide some selective advantage in the environment and might also be associat- ed with pathogenicity (Pei et al. 2013, Franks et al. 2014). Previous studies have demonstrated that these determi- nants are involved in resistance to bacteriophages and co- doi: 10.1590/0074-02760140479 licins (Whelan et al. 1995), antiseptics and disinfectants Financial support: CAPES, FAPERJ, CNPq, UERJ (SR-2/UERJ), (Teitzel & Parsek 2003) and antimicrobials (Collins et al. PNPD-CAPES/MEC, PAPD-FAPERJ/CAPES 2010, Pei et al. 2013, Franks et al. 2014). In addition, these LSS and CAA contributed equally to this work. + Corresponding author: [email protected] genes have also been implicated in adherence to epithelial Received 17 December 2014 cells (Yin et al. 2009, Pei et al. 2013) and susceptibility to Accepted 15 May 2015 reactive oxygen species (ROS) (Franks et al. 2014). online | memorias.ioc.fiocruz.br CDCE8392_0813 and diphtheria virulence • Louisy Sanches dos Santos et al. 663 : Currently, various virulence factors of C. diphtheriae 3 have been described, including the production of potent TeO 2 exotoxin, the formation of biofilms (Gomes et al. 2009), adherence, invasion and survival within different types of human cells (Hirata Jr et al. 2002, Bertuccini et al. 2004, cells]; cells]; K (2009) (1999), (1999), Santos et al. 2010, Peixoto et al. 2014). The major aetiologic (2003), R This paper References agent of diphtheria is also one of the most well-known Te Gomes et al. (2002, 2004), Moreira et al. pathogens. However, the mechanisms involved in this re- Hirata et Jr al. sistance and its relevance in the pathogenicity of C. diph- Mattos-Guaraldi et al. -hexadecane; CDC: Centres-hexadecane; CDC: theriae remain unknown. Therefore, in the present study, n we detected a putative TeR determinant in C. diphtheriae strain CDC-E8392 (CDCE8392_0813 protein) and showed a role for this gene in C. diphtheriae infection, analysing its DA DA pattern adherence effects on resistance to antimicrobial agents and hydrogen HEp-2 cells peroxide (H2O2), adherence to biotic and abiotic surfaces, intracellular survival and ability to kill nematodes. MATERIALS AND METHODS - /++ - /++ Glass/ Bacterial strains and growth conditions - C. diphthe- adherence riae strains used in this study and their characteristics are polystyrene listed in Table I. These microorganisms were maintained TM bacterial adherencetest;BATH: to in trypticase soy broth (TSB) (BD Difco , USA) at 37ºC t (%) and stored in the same medium with 20% glycerol. Es- BATH 51 ± 1.20 51 cherichia coli TOP10 Electrocomp™ (Thermo Fisher ± 0.82 51 Scientific Inc InvitrogenTM, USA) and E. coli OP50 were b strains used in this study TM grown in Luria Bertani (BD Difco ) medium at 37ºC. 3 When appropriate, kanamycin (Sigma-Aldrich Co, USA) TeO -1 2 was added (50 μg mL ). (mm) K 23 ± 1.15 23 27 ± 0.41 27 In silico search and three-dimensional model predic- inhibition halo R tion of the putative Te protein - An in silico search for re- ) 1 sistance determinants in C. diphtheriae strains was con- 3 TABLE I TABLE TeO 2 : p < 0.05 accordingunpaired to 0.05 < p : 0.31 ducted through the Protein Bank of the National Center 0.62 MIC b for Biotechnology Information. A hypothetical protein K (mg/mL- included in the TeO 2- resistance/dicarboxylate transport- 3 - er family was identified in all sequenced strains. A + Corynebacterium diphtheriae teh Inter The Phyre2 server was used to predict the three-dimen- rupted sional structure of the putative TeR protein of C. diphtheriae (Kelley & Sternberg 2009, Guo et al. 2012, Torktaz et al. a + + tox 2012, Nema & Pal 2013). Two parameters were considered gene to select the best model: confidence and coverage. R Disruption of the putative Te gene - For the chromo- 2008); (Pimentaal.gene et R somal disruption of the C. diphtheriae putative Te gene, tox ® ® the TOPO TA Cloning Kit (Thermo Fisher Scientific propertiesBiological of Biovar/ TM sucrose mitis/suc - mitis/suc - Inc Invitrogen ) was used. The CDC-E8392 strain was fermentation chosen as template and a 207 bp internal DNA fragment from CDCE8392_0813 gene was amplified via poly- merase chain reaction (PCR) with the following primer pair: 5’-TCGTTTTATGCGGGTGC-3’ and 5’-GGTGT- GCGCAATCTGATG-3’. Amplification was performed with an initial denaturation step at 94ºC for 2 min, fol- lowed by 35 cycles of denaturation at 94ºC for 1 min, an- Origin nealing at 60ºC for 1 min and extension at 72ºC for 1 min and 30 s and a final elongation step at 72ºC for 10 min. MIC: minimalMIC: inhibitory concentration; positive; ++: negative; +: moderately -: adherent to glass or polystyrene. The DNA fragment was ligated to the overhanging 3’- CDC-E8392::pCR2.1- TOPO’CDC-E8392_813’’ deoxythymidine of linearised pCR2.1-TOPO vector pro- Diphtheria/pharynx (USA) vided in the kit. The resulting plasmid “pCR2.1-TOPO- CDCE8392_0813” was propagated in E. coli TOP10 Electrocomp™ according to the manufacturer’s instruc- tions and isolated using the PureLink Quick DNA Mini- TM polymerasetoxicityevaluated by chainreaction: for prep Kit (Thermo Fisher Scientific Inc Invitrogen ). Five Strain LDCIC-L1 CDC-E8392 a for Disease Control and Prevention; diffuseDA: adherence [characterised by bacteria randomly distributedpotassium tellurite; over the surfaces of the human epithelial
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