Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains

Author:

Benevides Valdinete P.123ORCID,Saraiva Mauro M. S.23ORCID,Nascimento Camila F.2ORCID,Delgado-Suárez Enrique J.4ORCID,Oliveira Celso J. B.56ORCID,Silva Saura R.7ORCID,Miranda Vitor F. O.7ORCID,Christensen Henrik3,Olsen John E.3ORCID,Berchieri Junior Angelo2

Affiliation:

1. Postgraduate Program in Agricultural Microbiology, School of Agricultural and Veterinarian Sciences, São Paulo State University (Unesp), Jaboticabal 14884-900, Brazil

2. Department of Pathology, Reproduction and One Health, School of Agricultural and Veterinarian Sciences, São Paulo State University (Unesp), Jaboticabal 14884-900, Brazil

3. Department of Veterinary and Animal Sciences, University of Copenhagen, 1870 Frederiksberg, Denmark

4. Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México (UNAM), Mexico City 04510, Mexico

5. Center for Agricultural Sciences, Department of Animal Science, Federal University of Paraiba (CCA/UFPB), Areia 58051-900, Brazil

6. Global One Health Initiative (GOHi), The Ohio State University, Columbus, OH 43210, USA

7. Laboratory of Plant Systematics, Department of Biology, School of Agricultural and Veterinarian Sciences, São Paulo State University (Unesp), Jaboticabal 14884-900, Brazil

Abstract

In recent years, Salmonella enterica subsp. enterica serovar Mbandaka (S. Mbandaka) has been increasingly isolated from laying hens and shell eggs around the world. Moreover, this serovar has been identified as the causative agent of several salmonellosis outbreaks in humans. Surprisingly, little is known about the characteristics of this emerging serovar, and therefore, we investigated antimicrobial resistance, virulence, and prophage genes of six selected Brazilian strains of Salmonella Mbandaka using Whole Genome Sequencing (WGS). Multi-locus sequence typing revealed that the tested strains belong to Sequence Type 413 (ST413), which has been linked to recent multi-country salmonellosis outbreaks in Europe. A total of nine resistance genes were detected, and the most frequent ones were aac(6′)-Iaa, sul1, qacE, blaOXA-129, tet(B), and aadA1. A point mutation in ParC at the 57th position (threonine → serine) associated with quinolone resistance was present in all investigated genomes. A 112,960 bp IncHI2A plasmid was mapped in 4/6 strains. This plasmid harboured tetracycline (tetACDR) and mercury (mer) resistance genes, genes contributing to conjugative transfer, and genes involved in plasmid maintenance. Most strains (four/six) carried Salmonella genomic island 1 (SGI1). All S. Mbandaka genomes carried seven pathogenicity islands (SPIs) involved in intracellular survival and virulence: SPIs 1-5, 9, and C63PI. The virulence genes csgC, fimY, tcfA, sscA, (two/six), and ssaS (one/six) were absent in some of the genomes; conversely, fimA, prgH, and mgtC were present in all of them. Five Salmonella bacteriophage sequences (with homology to Escherichia phage phiV10, Enterobacteria phage Fels-2, Enterobacteria phage HK542, Enterobacteria phage ST64T, Salmonella phage SW9) were identified, with protein counts between 31 and 54, genome lengths of 24.7 bp and 47.7 bp, and average GC content of 51.25%. In the phylogenetic analysis, the genomes of strains isolated from poultry in Brazil clustered into well-supported clades with a heterogeneous distribution, primarily associated with strains isolated from humans and food. The phylogenetic relationship of Brazilian S. Mbandaka suggests the presence of strains with high epidemiological significance and the potential to be linked to foodborne outbreaks. Overall, our results show that isolated strains of S. Mbandaka are multidrug-resistant and encode a rather conserved virulence machinery, which is an epidemiological hallmark of Salmonella strains that have successfully disseminated both regionally and globally.

Funder

São Paulo Research Foundation

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

Publisher

MDPI AG

Subject

Virology,Microbiology (medical),Microbiology

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