Comparative Analysis of Genetic Determinants Encoding Cadmium, Arsenic, and Benzalkonium Chloride Resistance in Listeria monocytogenes of Human, Food, and Environmental Origin

Gelbíčová, Tereza; Florianová, Martina; Hlucháňová, Lucie; Kalová, Alžběta; Korena, Kristyna; Straková, Nicol; Karpíšková, Renata

doi:10.3389/fmicb.2020.599882

Cited by 23 publications

(28 citation statements)

References 35 publications

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“…According to several authors, the other remaining CCs detected in this study were previously isolated from different sources, such as food and environments [10,45,46,48,[52][53][54][55][56][57].…”

Section: Distribution Of Ccs and Cg-mlst Clusters And Their Virulence And Stress Resistance Profilesmentioning

confidence: 72%

Intensive Environmental Surveillance Plan for Listeria monocytogenes in Food Producing Plants and Retail Stores of Central Italy: Prevalence and Genetic Diversity

Centorotola

Guidi

D'Aurizio³

et al. 2021

Foods

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Listeria monocytogenes (Lm) can persist in food processing environments (FPEs), surviving environmental stresses and disinfectants. We described an intensive environmental monitoring plan performed in Central Italy and involving food producing plants (FPPs) and retail grocery stores (RSs). The aim of the study was to provide a snapshot of the Lm circulation in different FPEs during a severe listeriosis outbreak, using whole genome sequencing (WGS) to investigate the genetic diversity of the Lm isolated, evaluating their virulence and stress resistance profiles. A total of 1217 samples were collected in 86 FPEs with 12.0% of positive surfaces at FPPs level and 7.5% at RSs level; 133 Lm isolates were typed by multilocus sequencing typing (MLST) and core genome MLST (cgMLST). Clonal complex (CC) 121 (25.6%), CC9 (22.6%), CC1 (11.3%), CC3 (10.5%), CC191 (4.5%), CC7 (4.5%) and CC31 (3.8%) were the most frequent MLST clones. Among the 26 cgMLST clusters obtained, 5 of them persisted after sanitization and were re-isolated during the follow-up sampling. All the CC121 harboured the Tn6188_qac gene for tolerance to benzalkonium chloride and the stress survival islet SSI-2. The CC3, CC7, CC9, CC31 and CC191 carried the SSI-1. All the CC9 and CC121 strains presented a premature stop codon in the inlA gene. In addition to the Lm Pathogenicity Island 1 (LIPI-1), CC1, CC3 and CC191 harboured the LIPI-3. The application of intensive environmental sampling plans for the detection and WGS analysis of Lm isolates could improve surveillance and early detection of outbreaks.

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Section: Distribution Of Ccs and Cg-mlst Clusters And Their Virulence And Stress Resistance Profilesmentioning

confidence: 72%

Intensive Environmental Surveillance Plan for Listeria monocytogenes in Food Producing Plants and Retail Stores of Central Italy: Prevalence and Genetic Diversity

Centorotola

Guidi

D'Aurizio³

et al. 2021

Foods

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“…Heavy metals such as cadmium can be used in various pesticide products (including sanitizers) and therefore are commonly found in soils, and agricultural environments. Bacterial populations within these environments, such as L. monocytogenes, often possess genetic elements to combat this stressor [47,48]. These genes are commonly found on mobile genetic elements, such as plasmids (e.g., pLM80) or transposons (e.g., Tn5422), and their proximity in coding regions to QAC tolerance determinants (e.g., bcrABC) has led to speculation that the two may be associated.…”

Section: Discussionmentioning

confidence: 99%

“…The presence of cad did not seem to impact QAC tolerance. In evaluating isolates from food products, clinical cases, and environmental samples for QAC and heavy metal resistance genes, Gelbicova, et al [48] found that cadmium resistance determinants were more frequently found across the samples compared to QAC tolerance genes (27.8% vs. 7%). While the prevalence rate of cadmium resistance and QAC tolerance genes was similar in the present sample set, the combination of both gene types was not found in any one isolate (i.e., isolates with bcrABC did not have either cadA1 or cadA2).…”

Section: Discussionmentioning

confidence: 99%

Application of Whole Genome Sequencing to Understand Diversity and Presence of Genes Associated with Sanitizer Tolerance in Listeria monocytogenes from Produce Handling Sources

Bland

Johnson

Waite‐Cusic

et al. 2021

Foods

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Recent listeriosis outbreaks linked to fresh produce suggest the need to better understand and mitigate L. monocytogenes contamination in packing and processing environments. Using whole genome sequencing (WGS) and phenotype screening assays for sanitizer tolerance, we characterized 48 L. monocytogenes isolates previously recovered from environmental samples in five produce handling facilities. Within the studied population there were 10 sequence types (STs) and 16 cgMLST types (CTs). Pairwise single nucleotide polymorphisms (SNPs) ranged from 0 to 3047 SNPs within a CT, revealing closely and distantly related isolates indicative of both sporadic and continuous contamination events within the facility. Within Facility 1, we identified a closely related cluster (0–2 SNPs) of isolates belonging to clonal complex 37 (CC37; CT9492), with isolates recovered during sampling events 1-year apart and in various locations inside and outside the facility. The accessory genome of these CC37 isolates varied from 94 to 210 genes. Notable genetic elements and mutations amongst the isolates included the bcrABC cassette (2/48), associated with QAC tolerance; mutations in the actA gene on the Listeria pathogenicity island (LIPI) 1 (20/48); presence of LIPI-3 (21/48) and LIPI-4 (23/48). This work highlights the potential use of WGS in tracing the pathogen within a facility and understanding properties of L. monocytogenes in produce settings.

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“…LGI2 and LGI2-like islands appear to be uncommon in L. monocytogenes serotypes other than 4b, and arsenic resistance in serotypes 1/2a and 1/2c is frequently mediated by Tn554 [21,24]. Even more surprisingly, LGI2 and its variants have until now appeared to be restricted to L. monocytogenes.…”

Section: Introductionmentioning

confidence: 99%

“…LGI2 was originally identified in serotype 4b CC2 strain Scott A and harbors a cadmium resistance cassette (cadA4C4) that conferred resistance to lower levels of cadmium (35 µg/mL) in comparison to other cadAC cassettes (70 µg/mL) [21][22][23]. Further studies revealed that LGI2 was harbored by diverse strains of L. monocytogenes, with a predilection for the serotype 4b hypervirulent clones CC1 and CC2 [9,21,24].…”

Section: Introductionmentioning

confidence: 99%

Identification and Characterization of a Novel Genomic Island Harboring Cadmium and Arsenic Resistance Genes in Listeria welshimeri

et al. 2021

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Listeria monocytogenes, the bacterial foodborne pathogen responsible for the severe disease listeriosis, frequently exhibits heavy metal resistance. Concurrent resistance to cadmium and arsenic in L. monocytogenes is strongly associated with the 35-kb chromosomal island LGI2. LGI2 has been encountered repeatedly among L. monocytogenes serotype 4b hypervirulent clones but, surprisingly, not among non-pathogenic Listeria spp. Here we describe a novel LGI2 variant, LGI2-3, in two L. welshimeri strains from an urban aquatic environment. Whole genome sequence analysis revealed that the genomes were closely related except for one prophage region and confirmed a chromosomally integrated LGI2-3. It harbored a cystathionine beta-lyase gene previously only encountered in LGI2-1 of L. monocytogenes clonal complex 1 but was otherwise most closely related to LGI2. LGI2-3 harbored a novel cadAC cassette (cadA7C7) that, like LGI2′s cadA4C4, was associated with lower-level tolerance to cadmium (MIC 50 μg/mL) than other cadAC cassettes (MIC ≥ 140 μg/mL). CadA sequence analysis identified two amino acids that may be important for mediating different levels of cadmium tolerance. Our findings clearly demonstrated the potential for LGI2-like islands to be harbored by non-pathogenic Listeria spp. and generate intriguing hypotheses on the genetic diversity mediated by this island and its transfer among Listeria spp.

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Comparative Analysis of Genetic Determinants Encoding Cadmium, Arsenic, and Benzalkonium Chloride Resistance in Listeria monocytogenes of Human, Food, and Environmental Origin

Cited by 23 publications

References 35 publications

Intensive Environmental Surveillance Plan for Listeria monocytogenes in Food Producing Plants and Retail Stores of Central Italy: Prevalence and Genetic Diversity

Intensive Environmental Surveillance Plan for Listeria monocytogenes in Food Producing Plants and Retail Stores of Central Italy: Prevalence and Genetic Diversity

Application of Whole Genome Sequencing to Understand Diversity and Presence of Genes Associated with Sanitizer Tolerance in Listeria monocytogenes from Produce Handling Sources

Identification and Characterization of a Novel Genomic Island Harboring Cadmium and Arsenic Resistance Genes in Listeria welshimeri

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