Profiling the Virulence and Antibiotic Resistance Genes of Cronobacter sakazakii Strains Isolated From Powdered and Dairy Formulas by Whole-Genome Sequencing
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
34276629
PubMed Central
PMC8278472
DOI
10.3389/fmicb.2021.694922
Knihovny.cz E-zdroje
- Klíčová slova
- CRISPR-cas, Cronobacter sakazakii, antibiotic resistance genes, powdered formula, virulence,
- Publikační typ
- časopisecké články MeSH
Cronobacter sakazakii is an enteropathogen that causes neonatal meningitis, septicemia, and necrotizing enterocolitis in preterm infants and newborns with a mortality rate of 15 to 80%. Powdered and dairy formulas (P-DF) have been implicated as major transmission vehicles and subsequently the presence of this pathogen in P-DF led to product recalls in Chile in 2017. The objective of this study was to use whole genome sequencing (WGS) and laboratory studies to characterize Cronobacter strains from the contaminated products. Seven strains were identified as C. sakazakii, and the remaining strain was Franconibacter helveticus. All C. sakazakii strains adhered to a neuroblastoma cell line, and 31 virulence genes were predicted by WGS. The antibiograms varied between strains. and included mcr-9.1 and bla CSA genes, conferring resistance to colistin and cephalothin, respectively. The C. sakazakii strains encoded I-E and I-F CRISPR-Cas systems, and carried IncFII(pECLA), Col440I, and Col(pHHAD28) plasmids. In summary, WGS enabled the identification of C. sakazakii strains and revealed multiple antibiotic resistance and virulence genes. These findings support the decision to recall the contaminated powdered and dairy formulas from the Chilean market in 2017.
Department of Nutrition and Public Health Universidad del Bío Bío Chillán Chile
Department of Public Health Palacký University Olomouc Olomouc Czechia
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Aldubyan M., Almami I., Benslimane F., Alsonosi A., Forsythe S. (2017). Comparative outer membrane protein analysis of high and low-invasive strains of PubMed DOI PMC
Aly M. A., Domig K. J., Kneifel W., Reimhult E. (2019). Whole genome sequencing-based comparison of food isolates of PubMed DOI PMC
Baldwin A., Loughlin M., Caubilla-Barron J., Kucerova E., Manning G., Dowson C., et al. (2009). Multilocus sequence typing of PubMed DOI PMC
Bankevich A., Nurk S., Antipov D., Gurevich A., Dvorkin M., Kulikov A., et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. PubMed PMC
Baumgartner A., Grand M., Liniger M., Iversen C. (2009). Detection and frequency of PubMed DOI
Biswas A., Staals R., Morales S., Fineran P., Brown C. (2016). CRISPRDetect: a flexible algorithm to define CRISPR arrays. PubMed DOI PMC
Bolger A., Lohse M., Usadel B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. PubMed DOI PMC
Borowiak M., Baumann B., Fischer J., Thomas K., Deneke C., Hammerl J. A., et al. (2020). Development of a novel PubMed DOI PMC
Carattoli A., Zankari E., García-Fernández A., Voldby Larsen M., Lund O., Villa L., et al. (2014). In silico detection and typing of plasmids using plasmid finder and plasmid multilocus sequence typing. PubMed DOI PMC
Carroll L., Gaballa A., Guldimann C., Sullivan G., Henderson L., Wiedmann M. (2019). Identification of novel mobilized colistin resistance gene PubMed DOI PMC
Carter L., Lindsey L. A., Grim C. J., Sathyamoorthy V., Jarvis K. G., Gopinath G., et al. (2013). Multiplex PCR assay targeting a diguanylate cyclase-encoding gene, cgcA, to differentiate species within the genus PubMed DOI PMC
Caubilla-Barron J., Forsythe S. (2007). Dry stress and survival time of PubMed DOI
Chandrapala D., Kim K., Choi Y., Senevirathne A., Kang D., Ryu S., et al. (2014). Putative PubMed DOI PMC
Chase H. R., Gopinath G. R., Eshwar A. K., Stoller A., Fricker-Feer C., Gangiredla J., et al. (2017). Comparative genomic characterization of the highly persistent and potentially virulent PubMed DOI PMC
Chon J., Song K., Kim S., Hyeon J., Seo K. (2012). Isolation and characterization of PubMed DOI
Clinical and Laboratory Standards Institute [CLSI] (2018).
Couvin D., Bernheim A., Toffano-Nioche C., Touchon M., Michalik J., Néron B., et al. (2018). CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. PubMed DOI PMC
Cruz A., Xicohtencatl J., Gonzalez B., Bobadilla M., Eslava C., Rosas I. (2011). Virulence traits in PubMed DOI
Deter H. S., Jensen R. V., Mather W. H., Butzin N. C. (2017). Mechanisms for differential protein production in toxin–antitoxin systems. PubMed DOI PMC
Dingle T. C., Mulvey G. L., Armstrong G. D. (2011). Mutagenic analysis of the Clostridium difficile Flagellar proteins, FliC and FliD, and their contribution to virulence in Hamsters. PubMed DOI PMC
Falagas M., Athanasaki F., Voulgaris G., Triarides N., Vardakas K. (2019). Resistance to fosfomycin: mechanisms, frequency and clinical consequences. PubMed DOI
Fei P., Jiang Y., Feng J., Forsythe S. J., Li R., Zhou Y., et al. (2017). Antibiotic and desiccation resistance of PubMed DOI PMC
Fei P., Man C., Lou B., Forsythe S., Chai Y., Li R., et al. (2015). Genotyping and source tracking of the PubMed DOI PMC
Finkelstein S., Negrete F., Jang H., Gangiredla J., Mammel M., Patel I. R., et al. (2019). Prevalence, distribution, and phylogeny of type two toxin-antitoxin genes possessed by PubMed DOI PMC
Flores J. P., Arvizu S., Silva J., Fernández E. (2011). Two cases of hemorrhagic diarrhea caused by PubMed DOI
Forsythe S. J. (2018). Updates on the PubMed DOI
Forsythe S. J., Dickins B., Jolley K. A. (2014). PubMed DOI PMC
Franco A. A., Kothary M., Gopinath G., Jarvis K., Grim C. J., Hu L., et al. (2011). Cpa, the outer membrane protease of PubMed DOI PMC
Hariri S., Joseph S., Forsythe S. J. (2013). PubMed DOI PMC
Himelright I., Harris E., Lorch V., Anderson M. (2002). DOI
Hoeflinger J. L., Miller M. J. (2017). PubMed DOI PMC
Holý O., Cruz-Cordova A., Xicohtencatl-Cortés J., Hochel I., Parra-Flores J., Petrzelova J., et al. (2019). Occurrence of virulence factors in PubMed DOI
Holý O., Forsythe S. J. (2014). PubMed DOI
Holý O., Parra-Flores J., Lepuschitz S., Alarcón-Lavín M. P., Cruz-Córdova A., Xicohtencatl-Cortes J., et al. (2021). Molecular characterization of PubMed DOI PMC
Hunter C., Bean J. (2013). Cronobacter: an emerging opportunistic pathogen associated with neonatal meningitis, sepsis and necrotizing enterocolitis. PubMed DOI
Iversen C., Mullane N., Mc Cardell B., Tall B. D., Lehner A., Fanning S., et al. (2008). PubMed DOI
Jackson E., Forsythe S. J. (2016). Comparative study of PubMed DOI PMC
Jang H., Chase H. R., Gangiredla J., Grim C. J., Patel I. R., Kothary M. H., et al. (2020). Analysis of the molecular diversity among PubMed DOI PMC
Jia B., Raphenya A. R., Alcock B., Waglechner N., Guo P., Tsang K., et al. (2017). CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. PubMed DOI PMC
Johansson M., Bortolaia V., Tansirichaiya S., Aarestrup F., Roberts A., Petersen T. (2021). Detection of mobile genetic elements associated with antibiotic resistance in PubMed DOI PMC
Joseph S., Cetinkaya E., Drahovska H., Levican A., Figueras M., Forsythe S. (2012). PubMed DOI
Joseph S., Forsythe S. (2012). Insights into the emergent bacterial pathogen PubMed DOI PMC
Khezri A., Avershina E., Ahmad R. (2021). Plasmid identification and plasmid-mediated antimicrobial gene detection in norwegian isolates. PubMed DOI PMC
Kieffer N., Royer G., Decousser J. W., Bourrel A. S., Palmieri M., Ortiz, et al. (2019). mcr-9, an inducible gene encoding an acquired phosphoethano-lamine transferase in PubMed DOI PMC
Kim K., Jang S., Kim S., Park J., Heu S., Ryu S. (2008). Prevalence and genetic diversity of PubMed DOI
Kim K., Kim K., Choi J., Lim-Jeong A., Lee J., Hwang S., et al. (2010). Outer membrane proteins a (OmpA) and x (OmpX) are essential for basolateral invasion of PubMed DOI PMC
Kleiman M., Allen S., Neal P., Reynolds J. (1981). Meningoencephalitis and compartmentalization of the cerebral ventricles caused by PubMed PMC
Lange S., Alkhnbashi O., Rose D., Will S., Backofen R. (2013). CRISPRmap: an automated classification of repeat conservation in prokaryotic adaptive immune systems. PubMed DOI PMC
Lee Y.-D., Park J., Chang H. (2012). Detection, antibiotic susceptibility and biofilm formation of DOI
Lehner A., Tall B. D., Fanning S., Srikumar S. (2018). DOI
Lehner A., Tasara T., Stephan R. (2004). 16S PubMed DOI PMC
Leopold S., Goering R., Witten A., Harmsen D., Mellmann A. (2014). Bacterial whole-genome sequencing revisited: portable, scalable, and standardized analysis for typing and detection of virulence and antibiotic resistance genes. PubMed DOI PMC
Lepuschitz S., Ruppitsch W., Pekard-Amenitsch S., Forsythe S. J., Cormican M., Mach R. L., et al. (2019). Multicenter study of PubMed DOI PMC
Lepuschitz S., Sorschag S., Springer B., Allerberger F., Ruppitsch W. (2017). Draft genome sequence of carbapenemase-producing PubMed DOI PMC
Ling N., Jiang Y., Zeng H., Ding Y., Forsythe S. (2021). Advances in our understanding and distribution of the PubMed DOI
Makarova K. S., Koonin E.V. (2015). “Annotation and classification of CRISPR-Cas systems,” in PubMed DOI PMC
Mange J. P., Stephan R., Borel L., Wild P., Kim K. S., Pospischil A., et al. (2006). Adhesive properties of PubMed DOI PMC
Mare A., Man A., Toma F., Ciurea C. N., Coşeriu R. L., Vintilă C., et al. (2020). Hemolysin-producing strains among diarrheagenic PubMed DOI PMC
Mazzantini D., Fonnesu R., Celandroni F., Calvigioni M., Vecchione A., Mrusek D., et al. (2020). GTP-dependent FlhF homodimer supports secretion of a hemolysin in PubMed DOI PMC
Mohan-Nair M. K., Venkitanarayanan K. S. (2006). Cloning and sequencing of the ompA gene of PubMed DOI PMC
Molloy C., Cagney C., O’Brien S., Iversen C., Fanning S., Duffy G. (2009). Surveillance and characterization by pulsed-field gel electrophoresis of PubMed DOI
Morato-Rodríguez M., Velandia-Rodríguez D., Castañeda S., Crosby M., Vera H. (2018). PubMed DOI PMC
Müller A., Hächler H., Stephan R., Lehner A. (2014). Presence of AmpC beta-lactamases, CSA-1, CSA-2, CMA-1, and CMA-2 Conferring an unusual resistance phenotype in PubMed DOI
Ogrodzki P., Forsythe S. (2015). Capsular profiling of the PubMed DOI PMC
Ogrodzki P., Forsythe S. (2016). CRISPR–cas loci profiling of PubMed DOI
Ogrodzki P., Forsythe S. (2017). DNA-sequence based typing of the PubMed DOI PMC
Parra J., Oliveras L., Rodriguez A., Riffo F., Jackson E., Forsythe S. (2015). Riesgo por DOI
Parra-Flores J., Aguirre J., Juneja V., Jackson E., Cruz-Córdova A., Silva-Sanchez J., et al. (2018a). Virulence and antibiotic resistance profiles of PubMed DOI PMC
Parra-Flores J., Cerda-Leal F., Contreras A., Valenzuela-Riffo N., Rodriguez A., Aguirre J. (2018b). PubMed DOI PMC
Parra-Flores J., Cruz-Córdova A., Acuña S., Riffo-Sepúlveda F., Maury-Sintjago E., Rodriguez-Fernández A., et al. (2021). “
Parra-Flores J., Maury-Sintjago E., Rodriguez-Fernández A., Acuña S., Cerda F., Aguirre J., et al. (2020). Microbiological quality of powdered infant formula in Latin America. PubMed DOI
Patrick M., Mahon B., Greene S., Rounds J., Conquist A., Wymore K., et al. (2014). Incidence of PubMed DOI PMC
Proudy I., Bouglé D., Coton E., Coton M., Leclercq R., Vergnaud M. (2008). Genotypic characterization of PubMed DOI
Ramsamy Y., Mlisana K. P., Allam M., Amoako D. G., Abia A. L. K., Ismail A., et al. (2020). Genomic analysis of carbapenemase-producing extensively drug-resistant PubMed DOI PMC
Severi E., Hood D. W., Thomas G. H. (2007). Sialic acid utilization by bacterial pathogens. PubMed DOI
Shi L., Liang Q., Zhan Z., Feng J., Zhao Y., Chen, et al. (2018). Co-occurrence of 3 different resistance plasmids in a multi-drug resistant PubMed DOI PMC
Sohanpal B. K., Friar S., Roobol J., Plumbridge J. A., Blomfield I. C. (2007). Multiple co-regulatory elements and IHF are necessary for the control of PubMed DOI
Sonbol H., Joseph S., McAuley C., Craven H., Forsythe S. (2013). Multilocus sequence typing of DOI
Stephan R., Grim C., Gopinath G., Mammel M., Sathyamoorthy V., Trach L., et al. (2014). Re-examination of the taxonomic status of PubMed DOI PMC
Stoop B., Lenher A., Iversen C., Fanning S. (2009). Development and evaluation of rpoB based PCR systems to differentiate the six proposed species within the genus PubMed DOI
Townsend S., Hurrell E., Gonzalez-Gomez I., Lowe J., Frye J., Forsythe S., et al. (2007). PubMed DOI
Veronica E.-K., Sara A. O., Everardo C. Q., Héctor Q., Oscar M. C., Elizabeth F. R., et al. (2020). Proteomics profiles of PubMed DOI
Vojkovska H., Karpiskova R., Orieskova M., Drahovska H. (2016). Characterization of PubMed DOI
Vornhagen J., Bassis C., Ramakrishnan S., Hein R., Mason S., Bergman Y., et al. (2020). A plasmid locus associated with PubMed DOI PMC
Walling L. R., Butler J. S. (2019). Toxins targeting transfer RNAs: translation inhibition by bacterial toxin–antitoxin systems. PubMed DOI PMC
Ye Y. W., Ling N., Jiao R., Wu Q. G., Han Y. J., Gao J. N. (2015). Effects of culture conditions on the biofilm formation of DOI
Zeng H., Lei T., He W., Zhang J., Liang B., Li C., et al. (2018). Novel multidrug resistant PubMed DOI PMC
Zeng H., Zhang J., Li C., Xie T., Ling N., Wu Q., et al. (2017). The driving force of prophages and CRISPR-Cas system in the evolution of PubMed DOI PMC