Genomic Sequencing of Bacillus cereus Sensu Lato Strains Isolated from Meat and Poultry Products in South Africa Enables Inter- and Intranational Surveillance and Source Tracking

ABSTRACT Members of the Bacillus cereus sensu lato species complex, also known as the B. cereus group, vary in their ability to cause illness but are frequently isolated from foods, including meat products; however, food safety surveillance efforts that use whole-genome sequencing (WGS) often neglec...

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Main Authors: Laura M. Carroll, Rian Pierneef, Aletta Mathole, Abimbola Atanda, Itumeleng Matle
Format: Article
Language:English
Published: American Society for Microbiology 2022-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.00700-22
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author Laura M. Carroll
Rian Pierneef
Aletta Mathole
Abimbola Atanda
Itumeleng Matle
author_facet Laura M. Carroll
Rian Pierneef
Aletta Mathole
Abimbola Atanda
Itumeleng Matle
author_sort Laura M. Carroll
collection DOAJ
description ABSTRACT Members of the Bacillus cereus sensu lato species complex, also known as the B. cereus group, vary in their ability to cause illness but are frequently isolated from foods, including meat products; however, food safety surveillance efforts that use whole-genome sequencing (WGS) often neglect these potential pathogens. Here, we evaluate the surveillance and source tracking potential of WGS as applied to B. cereus sensu lato by (i) using WGS to characterize B. cereus sensu lato strains isolated during routine surveillance of meat products across South Africa (n = 25) and (ii) comparing the genomes sequenced here to all publicly available, high-quality B. cereus sensu lato genomes (n = 2,887 total genomes). Strains sequenced here were collected from meat products obtained from (i) retail outlets, processing plants, and butcheries across six South African provinces (n = 23) and (ii) imports held at port of entry (n = 2). The 25 strains sequenced here were partitioned into 15 lineages via in silico seven-gene multilocus sequence typing (MLST). While none of the South African B. cereus sensu lato strains sequenced here were identical to publicly available genomes, six MLST lineages contained multiple strains sequenced in this study, which were identical or nearly identical at the whole-genome scale (≤3 core single nucleotide polymorphisms). Five MLST lineages contained (nearly) identical genomes collected from two or three South African provinces; one MLST lineage contained nearly identical genomes from two countries (South Africa and the Netherlands), indicating that B. cereus sensu lato can spread intra- and internationally via foodstuffs. IMPORTANCE Nationwide foodborne pathogen surveillance programs that use high-resolution genomic methods have been shown to provide vast public health and economic benefits. However, Bacillus cereus sensu lato is often overlooked during large-scale routine WGS efforts. Thus, to our knowledge, no studies to date have evaluated the potential utility of WGS for B. cereus sensu lato surveillance and source tracking in foodstuffs. In this preliminary proof-of-concept study, we applied WGS to B. cereus sensu lato strains collected via South Africa’s national surveillance program of domestic and imported meat products, and we provide strong evidence that B. cereus sensu lato can be disseminated intra- and internationally via the agro-food supply chain. Our results showcase that WGS has the potential to be used for source tracking of B. cereus sensu lato in foods, although future WGS and metadata collection efforts are needed to ensure that B. cereus sensu lato surveillance initiatives are on par with those of other foodborne pathogens.
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spelling doaj.art-fcd7aa83b97141dd9ec3edf664a9cc182022-12-22T02:39:00ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.00700-22Genomic Sequencing of Bacillus cereus Sensu Lato Strains Isolated from Meat and Poultry Products in South Africa Enables Inter- and Intranational Surveillance and Source TrackingLaura M. Carroll0Rian Pierneef1Aletta Mathole2Abimbola Atanda3Itumeleng Matle4Structural and Computational Biology Unit, EMBL, Heidelberg, GermanyBiotechnology Platform, Agricultural Research Council, Onderstepoort Veterinary Research, Onderstepoort, South AfricaBacteriology Division, Agricultural Research Council, Onderstepoort Veterinary Research, Onderstepoort, South AfricaBacteriology Division, Agricultural Research Council, Onderstepoort Veterinary Research, Onderstepoort, South AfricaBacteriology Division, Agricultural Research Council, Onderstepoort Veterinary Research, Onderstepoort, South AfricaABSTRACT Members of the Bacillus cereus sensu lato species complex, also known as the B. cereus group, vary in their ability to cause illness but are frequently isolated from foods, including meat products; however, food safety surveillance efforts that use whole-genome sequencing (WGS) often neglect these potential pathogens. Here, we evaluate the surveillance and source tracking potential of WGS as applied to B. cereus sensu lato by (i) using WGS to characterize B. cereus sensu lato strains isolated during routine surveillance of meat products across South Africa (n = 25) and (ii) comparing the genomes sequenced here to all publicly available, high-quality B. cereus sensu lato genomes (n = 2,887 total genomes). Strains sequenced here were collected from meat products obtained from (i) retail outlets, processing plants, and butcheries across six South African provinces (n = 23) and (ii) imports held at port of entry (n = 2). The 25 strains sequenced here were partitioned into 15 lineages via in silico seven-gene multilocus sequence typing (MLST). While none of the South African B. cereus sensu lato strains sequenced here were identical to publicly available genomes, six MLST lineages contained multiple strains sequenced in this study, which were identical or nearly identical at the whole-genome scale (≤3 core single nucleotide polymorphisms). Five MLST lineages contained (nearly) identical genomes collected from two or three South African provinces; one MLST lineage contained nearly identical genomes from two countries (South Africa and the Netherlands), indicating that B. cereus sensu lato can spread intra- and internationally via foodstuffs. IMPORTANCE Nationwide foodborne pathogen surveillance programs that use high-resolution genomic methods have been shown to provide vast public health and economic benefits. However, Bacillus cereus sensu lato is often overlooked during large-scale routine WGS efforts. Thus, to our knowledge, no studies to date have evaluated the potential utility of WGS for B. cereus sensu lato surveillance and source tracking in foodstuffs. In this preliminary proof-of-concept study, we applied WGS to B. cereus sensu lato strains collected via South Africa’s national surveillance program of domestic and imported meat products, and we provide strong evidence that B. cereus sensu lato can be disseminated intra- and internationally via the agro-food supply chain. Our results showcase that WGS has the potential to be used for source tracking of B. cereus sensu lato in foods, although future WGS and metadata collection efforts are needed to ensure that B. cereus sensu lato surveillance initiatives are on par with those of other foodborne pathogens.https://journals.asm.org/doi/10.1128/spectrum.00700-22Bacillus anthracisBacillus cereusBacillus cereus groupBacillus paranthracisBacillus thuringiensisBacillus wiedmannii
spellingShingle Laura M. Carroll
Rian Pierneef
Aletta Mathole
Abimbola Atanda
Itumeleng Matle
Genomic Sequencing of Bacillus cereus Sensu Lato Strains Isolated from Meat and Poultry Products in South Africa Enables Inter- and Intranational Surveillance and Source Tracking
Microbiology Spectrum
Bacillus anthracis
Bacillus cereus
Bacillus cereus group
Bacillus paranthracis
Bacillus thuringiensis
Bacillus wiedmannii
title Genomic Sequencing of Bacillus cereus Sensu Lato Strains Isolated from Meat and Poultry Products in South Africa Enables Inter- and Intranational Surveillance and Source Tracking
title_full Genomic Sequencing of Bacillus cereus Sensu Lato Strains Isolated from Meat and Poultry Products in South Africa Enables Inter- and Intranational Surveillance and Source Tracking
title_fullStr Genomic Sequencing of Bacillus cereus Sensu Lato Strains Isolated from Meat and Poultry Products in South Africa Enables Inter- and Intranational Surveillance and Source Tracking
title_full_unstemmed Genomic Sequencing of Bacillus cereus Sensu Lato Strains Isolated from Meat and Poultry Products in South Africa Enables Inter- and Intranational Surveillance and Source Tracking
title_short Genomic Sequencing of Bacillus cereus Sensu Lato Strains Isolated from Meat and Poultry Products in South Africa Enables Inter- and Intranational Surveillance and Source Tracking
title_sort genomic sequencing of bacillus cereus sensu lato strains isolated from meat and poultry products in south africa enables inter and intranational surveillance and source tracking
topic Bacillus anthracis
Bacillus cereus
Bacillus cereus group
Bacillus paranthracis
Bacillus thuringiensis
Bacillus wiedmannii
url https://journals.asm.org/doi/10.1128/spectrum.00700-22
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