Comparative genomics reveals high genetic similarity among strains of Salmonella enterica serovar Infantis isolated from multiple sources in Brazil

Felipe P Vilela; Andrei G Felice; Amanda A Seribelli; Dália P Rodrigues; Siomar C Soares; Marc W Allard; Juliana P Falcão

doi:10.7717/peerj.17306

Comparative genomics reveals high genetic similarity among strains of Salmonella enterica serovar Infantis isolated from multiple sources in Brazil

PeerJ. 2024 May 20:12:e17306. doi: 10.7717/peerj.17306. eCollection 2024.

Authors

Felipe P Vilela¹, Andrei G Felice², Amanda A Seribelli³, Dália P Rodrigues⁴, Siomar C Soares², Marc W Allard⁵, Juliana P Falcão¹

Affiliations

¹ School of Pharmaceutical Sciences of Ribeirão Preto, Department of Clinical Analyses, Toxicology and Food Science, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil.
² Institute of Biological and Natural Sciences, Department of Microbiology, Immunology and Parasitology, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil.
³ Medical School of Ribeirão Preto, Department of Cellular and Molecular Biology, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil.
⁴ Oswaldo Cruz Institute, Fundação Oswaldo Cruz, Rio de Janeiro, Rio de Janeiro, Brazil.
⁵ Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration, College Park, MD, United States of America.

Abstract

Background: Salmonella enterica serovar Infantis (Salmonella Infantis) is a zoonotic, ubiquitous and foodborne pathogen of worldwide distribution. Despite Brazil's relevance as a major meat exporter, few studies were conducted to characterize strains of this serovar by genomic analyses in this country. Therefore, this study aimed to assess the diversity of 80 Salmonella Infantis strains isolated from veterinary, food and human sources in Brazil between 2013 and 2018 by comparative genomic analyses. Additional genomes of non-Brazilian countries (n = 18) were included for comparison purposes in some analyses.

Methods: Analyses of whole-genome multi-locus sequence typing (wgMLST), using PGAdb-builder, and of fragmented genomes, using Gegenees, were conducted to compare the 80 Brazilian strains to the 18 non-Brazilian genomes. Pangenome analyses and calculations were performed for all Salmonella Infantis genomes analyzed. The presence of prophages was determined using PHASTER for the 80 Brazilian strains. The genome plasticity using BLAST Ring Image Generator (BRIG) and gene synteny using Mauve were evaluated for 20 selected Salmonella Infantis genomes from Brazil and ten from non-Brazilian countries. Unique orthologous protein clusters were searched in ten selected Salmonella Infantis genomes from Brazil and ten from non-Brazilian countries.

Results: wgMLST and Gegenees showed a high genomic similarity among some Brazilian Salmonella Infantis genomes, and also the correlation of some clusters with non-Brazilian genomes. Gegenees also showed an overall similarity >91% among all Salmonella Infantis genomes. Pangenome calculations revealed an open pangenome for all Salmonella Infantis subsets analyzed and a high gene content in the core genomes. Fifteen types of prophages were detected among 97.5% of the Brazilian strains. BRIG and Mauve demonstrated a high structural similarity among the Brazilian and non-Brazilian isolates. Unique orthologous protein clusters related to biological processes, molecular functions, and cellular components were detected among Brazilian and non-Brazilian genomes.

Conclusion: The results presented using different genomic approaches emphasized the significant genomic similarity among Brazilian Salmonella Infantis genomes analyzed, suggesting wide distribution of closely related genotypes among diverse sources in Brazil. The data generated contributed to novel information regarding the genomic diversity of Brazilian and non-Brazilian Salmonella Infantis in comparison. The different genetically related subtypes of Salmonella Infantis from Brazil can either occur exclusively within the country, or also in other countries, suggesting that some exportation of the Brazilian genotypes may have already occurred.

Keywords: Comparative genomics; Gegenees; Pangenome analysis; Prophages; Salmonella Infantis; Whole-genome sequencing; wgMLST.

Publication types

Comparative Study

MeSH terms

Animals
Brazil
Food Microbiology
Genome, Bacterial* / genetics
Genomics*
Humans
Multilocus Sequence Typing*
Phylogeny
Salmonella Infections / epidemiology
Salmonella Infections / microbiology
Salmonella Infections, Animal / epidemiology
Salmonella Infections, Animal / microbiology
Salmonella enterica* / genetics
Salmonella enterica* / isolation & purification
Serogroup

Grants and funding

This study was supported by research grants from the FDA/Center for Food Safety and Applied Nutrition (CFSAN) under the supervision of Marc W Allard and from the São Paulo Research Foundation (FAPESP; Proc. 2019/19338-8) under the supervision of Juliana P. Falcão. During the course of this work, Felipe P. Vilela was supported by Master and PhD student scholarships from FAPESP (Proc. 2019/06947-6) and the National Council for Scientific and Technological Development (CNPq; Proc. 141017/2021-0), respectively. Juliana P. Falcão also received Productive fellowships from CNPq (Proc. 304399/2018-3 and 304803/2021-9). This study was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.