Characterization of Emetic and Diarrheal Bacillus cereus Strains From a 2016 Foodborne Outbreak Using Whole-Genome Sequencing: Addressing the Microbiological, Epidemiological, and Bioinformatic Challenges

Carroll, Laura M.; Mukherjee, Manjarí; Nicholas, David; Mingle, Lisa A.; Dumas, Nellie B.; Cole, Jocelyn A.; Kovač, Jasna

doi:10.3389/fmicb.2019.00144

Cited by 93 publications

(88 citation statements)

References 89 publications

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“…Current species definitions cannot reliably differentiate B. anthracis from neighboring lineages. The practice of calculating ANI values between a genome of interest and the genomes of known B. cereus group species type strains (see Table S1 in the supplemental material) (33)(34)(35)39) and using the widely accepted threshold of 95 ANI (5) as a hard genomospecies cutoff produced nonoverlapping genomospecies clusters for Bacillus albus, "B. bingmayongensis," B. cytotoxicus, "B. gaemokensis," B. luti, "B. manliponensis," B. nitratireducens, B. paramycoides, B. proteolyticus, B. pseudomycoides, and B. toyonensis (Table S2). No genomes assigned to these genomospecies shared Ն95 ANI with any genomes assigned to a different genomospecies ( Fig.…”

Section: Resultsmentioning

confidence: 99%

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Proposal of a Taxonomic Nomenclature for the Bacillus cereus Group Which Reconciles Genomic Definitions of Bacterial Species with Clinical and Industrial Phenotypes

Carroll¹,

Wiedmann

Kovač

2020

mBio

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136

231

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The Bacillus cereus group comprises numerous closely related species, including bioterrorism agent B. anthracis, foodborne pathogen B. cereus, and biopesticide B. thuringiensis. Differentiating organisms capable of causing illness or death from those used in industry is essential for risk assessment and outbreak preparedness. However, current species definitions facilitate species-phenotype incongruences, particularly when horizontally acquired genes are responsible for a phenotype. Using all publicly available B. cereus group genomes (n = 2,231), we show that current species definitions lead to overlapping genomospecies clusters, in which 66.2% of genomes belong to multiple genomospecies at a conventional 95 average nucleotide identity (ANI) genomospecies threshold. A genomospecies threshold of ≈92.5 ANI is shown to reflect a natural gap in genome similarity for the B. cereus group, and medoid genomes identified at this threshold are shown to yield resolvable genomospecies clusters with minimal overlap (six of 2,231 genomes assigned to multiple genomospecies; 0.269%). We thus propose a nomenclatural framework for the B. cereus group which accounts for (i) genomospecies using resolvable genomospecies clusters obtained at ≈92.5 ANI, (ii) established lineages of medical importance using a formal collection of subspecies names, and (iii) heterogeneity of clinically and industrially important phenotypes using a formalized and extended collection of biovar terms. We anticipate that the proposed nomenclature will remain interpretable to clinicians, without sacrificing genomic species definitions, which can in turn aid in pathogen surveillance; early detection of emerging, high-risk genotypes; and outbreak preparedness. IMPORTANCE Historical species definitions for many prokaryotes, including pathogens, have relied on phenotypic characteristics that are inconsistent with genome evolution. This scenario forces microbiologists and clinicians to face a tradeoff between taxonomic rigor and clinical interpretability. Using the Bacillus cereus group as a model, a conceptual framework for the taxonomic delineation of prokaryotes which reconciles genomic definitions of species with clinically and industrially relevant phenotypes is presented. The nomenclatural framework outlined here serves as a model for genomics-based bacterial taxonomy that moves beyond arbitrarily set genomospecies thresholds while maintaining congruence with phenotypes and historically important species names.

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Section: Resultsmentioning

confidence: 99%

“…Further confusion arises when "novel" species encompass established lineages within their genomospecies thresholds. For example, B. paranthracis, a species published in 2017 (35), encompasses the established foodborne pathogen known as emetic "B. cereus" (13,(36)(37)(38) within its genomospecies boundaries at a conventional 95 ANI threshold (39).…”

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confidence: 99%

Proposal of a Taxonomic Nomenclature for the Bacillus cereus Group Which Reconciles Genomic Definitions of Bacterial Species with Clinical and Industrial Phenotypes

Carroll¹,

Wiedmann

Kovač

2020

mBio

Self Cite

136

231

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“…Gubbins version 2.2.0 62 was used to filter out recombination events from the consensus sequences, yielding a total of 5,254 SNPs among the 87 S. Typhimurium isolates, 4,774 of which were core SNPs. The variant calling pipeline described here has been implemented as the default pipeline in SNPBac version 1.0.0 (https ://githu b.com/lmc29 7/SNPBa c ) 63 .…”

Section: Methods Isolate Selection a Total Of 42 Isolates Availablementioning

confidence: 99%

Twentieth-century emergence of antimicrobial resistant human- and bovine-associated Salmonella enterica serotype Typhimurium lineages in New York State

Carroll

Huisman

2020

Sci Rep

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Salmonella enterica serotype typhimurium (S. typhimurium) boasts a broad host range and can be transmitted between livestock and humans. While members of this serotype can acquire resistance to antimicrobials, the temporal dynamics of this acquisition is not well understood. Using new York State (NYS) and its dairy cattle farms as a model system, 87 S. Typhimurium strains isolated from 1999 to 2016 from either human clinical or bovine-associated sources in NYS were characterized using wholegenome sequencing. More than 91% of isolates were classified into one of four major lineages, two of which were largely susceptible to antimicrobials but showed sporadic antimicrobial resistance (AMR) gene acquisition, and two that were largely multidrug-resistant (MDR). All four lineages clustered by presence and absence of elements in the pan-genome. the two MDR lineages, one of which resembled S. Typhimurium DT104, were predicted to have emerged circa 1960 and 1972. The two largely susceptible lineages emerged earlier, but showcased sporadic AMR determinant acquisition largely after 1960, including acquisition of cephalosporin resistance-conferring genes after 1985. These results confine the majority of AMR acquisition events in NYS S. typhimurium to the twentieth century, largely within the era of antibiotic usage. Salmonella enterica subsp. enterica serotype Typhimurium (S. Typhimurium) consistently ranks as one of the serotypes most commonly isolated from human clinical cases in the United States; in 2016, it was reported as being responsible for 4,581 culture-confirmed human infections in the U.S. alone 1. Additionally, S. Typhimurium is capable of infecting a broad range of hosts: it is frequently isolated not only from humans, but from animals as well, including livestock, rodents, and birds 2-4. Within the serotype, numerous S. Typhimurium lineages have been identified, several of which are notable due to their propensity for resistance to antimicrobials 5. Many of these lineages have been assigned using phage typing, a practice by which S. Typhimurium can be differentiated based on its susceptibility to lysis by phages of varying specificity 6. Host range can vary within phage type, as some phage types (e.g. DT104, DT204, DT49) are commonly associated with epidemics among livestock and humans 2,6,7 , while others exhibit a narrower host range (e.g. DT2 and DT99, which are highly virulent in pigeons) 6-9. Additionally, a number of S. Typhimurium lineages are often associated with distinct antimicrobial resistance (AMR) profiles; for example, S. Typhimurium DT104 is often characterized by its resistance to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline (ACSSuT), although AMR profiles within a lineage can vary 10-13. While whole-genome sequencing (WGS) is being increasingly employed to characterize S. Typhimurium from diverse sources at high resolution, the bulk of the effort has focused on characterizing distinct lineages that have been responsible for human epidemics (e.g. DT104) 12,14. Furt...

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“…Foodborne illness related to B. cereus appear as two distinct symptoms; diarrhoeal and emetic. Diarrhoeal symptoms often characterised as diarrhoea and abdominal pain, usually eight to 16 hours after consumption of contaminated food; whereas emetic symptoms can be observed as nausea and vomiting, usually one to five hours (Agata et al, 2002;Caroll et al, 2019). Back in 2013, a massive food poisoning outbreak related to enterotoxigenic B. cereus was reported by Schmid et al (2016).…”

Section: Introductionmentioning

confidence: 99%

Prevalence of Bacillus cereus s.l. in ultra-high temperature chocolate milk from selected milk manufacturers in Malaysia

Anyi¹,

New²,

Chai³

et al. 2020

Food Res.

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Bacillus cereus is a major foodborne pathogen of great concern to the dairy industry owing to its resilient spores as well as the adverse effect of its toxins. At present, there is no informational study available to solve or pinpoint the UHT chocolate milk contamination issue in Malaysia. This work aimed to investigate the prevalence and contamination level of B. cereus s.l. in UHT chocolate milk and to suggest the appropriate solution for the issue. In the present study, B. cereus s.l. prevalence and contamination level in individually packed UHT chocolate milk from processing factories was evaluated. The prevalence and concentration of B. cereus s.l. were determined via MPN-PCR (Most Probable Number-Polymerase Chain Reaction) assay. Results showed that 31.11% from 220 of UHT chocolate milk tested contained Bacillus spp.; of this Bacillus spp. positive samples, 24.30% were also positive for B. cereus s.l. with concentration ranging from less than 3 to more than 1100 MPN/mL. Findings from this study highlighted the possibility of UHT chocolate milk as a potential source of B. cereus s.l. infection. Therefore, findings emphasized the needs to revise, monitor and improve UHT sterilization process to reduce infection risk. Furthermore, it is also essential to maintain the hygiene to minimize initial microbial load and contamination of UHT chocolate milk, beginning from production to retail.

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Characterization of Emetic and Diarrheal Bacillus cereus Strains From a 2016 Foodborne Outbreak Using Whole-Genome Sequencing: Addressing the Microbiological, Epidemiological, and Bioinformatic Challenges

Cited by 93 publications

References 89 publications

Proposal of a Taxonomic Nomenclature for the Bacillus cereus Group Which Reconciles Genomic Definitions of Bacterial Species with Clinical and Industrial Phenotypes

Proposal of a Taxonomic Nomenclature for the Bacillus cereus Group Which Reconciles Genomic Definitions of Bacterial Species with Clinical and Industrial Phenotypes

Twentieth-century emergence of antimicrobial resistant human- and bovine-associated Salmonella enterica serotype Typhimurium lineages in New York State

Prevalence of Bacillus cereus s.l. in ultra-high temperature chocolate milk from selected milk manufacturers in Malaysia

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