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

Environmental adaptation of Listeria monocytogenes is a complex process involving various mechanisms that can contribute to their survival in the environment, further spreading throughout the food chain and the development of listeriosis. The aim of this study was to analyze whole-genome sequencing data in a set of 270 strains of L. monocytogenes derived from human listeriosis cases and food and environmental sources in order to compare the prevalence and type of genetic determinants encoding cadmium, arsenic, and benzalkonium chloride resistance. Most of the detected genes of cadmium (27.8%), arsenic (15.6%), and benzalkonium chloride (7.0%) resistance were located on mobile genetic elements, even in phylogenetically distant lineages I and II, which indicates the possibility of their horizontal spread. Although no differences were found in the prevalence of these genes between human and food strains, they have been detected sporadically in strains from the environment. Regarding cadmium resistance genes, cadA1C1_Tn5422 predominated, especially in clonal complexes (CCs) 121, 8, and 3 strains. At the same time, qacH_Tn6188-encoding benzalkonium chloride resistance was most frequently detected in the genome of CC121 strains. Genes encoding arsenic resistance were detected mainly in strains CC2 (located on the chromosomal island LGI2) and CC9 (carried on Tn554). The results indicated a relationship between the spread of genes encoding resistance to cadmium, arsenic, and benzalkonium chloride in certain serotypes and CCs and showed the need for a more extensive study of L. monocytogenes strains to better understand their ability to adapt to the food production environment.

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Prevalence of plasmid-borne benzalkonium chloride resistance cassette bcrABC and cadmium resistance cadA genes in nonpathogenic Listeria spp. isolated from food and food-processing environments

International Journal of Food Microbiology ◽

10.1016/j.ijfoodmicro.2018.10.019 ◽

2019 ◽

Vol 290 ◽

pp. 247-253 ◽

Cited By ~ 8

Author(s):

Dorota Korsak ◽

Cora Chmielowska ◽

Magdalena Szuplewska ◽

Dariusz Bartosik

Keyword(s):

Food Processing ◽

Benzalkonium Chloride ◽

Cadmium Resistance ◽

Chloride Resistance

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Genetic Determinants for Cadmium and Arsenic Resistance among Listeria monocytogenes Serotype 4b Isolates from Sporadic Human Listeriosis Patients

Applied and Environmental Microbiology ◽

10.1128/aem.03551-12 ◽

2013 ◽

Vol 79 (7) ◽

pp. 2471-2476 ◽

Cited By ~ 28

Author(s):

Sangmi Lee ◽

M. Rakic-Martinez ◽

L. M. Graves ◽

T. J. Ward ◽

R. M. Siletzky ◽

...

Keyword(s):

Heavy Metal ◽

Listeria Monocytogenes ◽

Heavy Metal Resistance ◽

Metal Resistance ◽

Genetic Determinants ◽

Chromosomal Locus ◽

Cadmium Resistance ◽

Arsenic Resistance ◽

Content Type ◽

Serotype 4B

ABSTRACTInListeria monocytogenesserotype 4b isolates from sporadic listeriosis, heavy metal resistance was primarily encountered in certain clonal groups (ECI, ECII, and ECIa). All arsenic-resistant isolates harbored the arsenic resistance cassette previously identified in pLI100; ECIa harbored additional arsenic resistance genes and a novel cadmium resistance determinant in a conserved chromosomal locus.

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Screening of benzalkonium chloride resistance in Listeria monocytogenes strains isolated during cold smoked fish production

Letters in Applied Microbiology ◽

10.1111/j.1472-765x.2005.01763.x ◽

2005 ◽

Vol 41 (3) ◽

pp. 291-296 ◽

Cited By ~ 50

Author(s):

C. Soumet ◽

C. Ragimbeau ◽

P. Maris

Keyword(s):

Listeria Monocytogenes ◽

Benzalkonium Chloride ◽

Fish Production ◽

Smoked Fish ◽

Chloride Resistance

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Conservation and Distribution of the Benzalkonium Chloride Resistance CassettebcrABCin Listeria monocytogenes

Applied and Environmental Microbiology ◽

10.1128/aem.01751-13 ◽

2013 ◽

Vol 79 (19) ◽

pp. 6067-6074 ◽

Cited By ~ 46

Author(s):

Vikrant Dutta ◽

Driss Elhanafi ◽

Sophia Kathariou

Keyword(s):

Listeria Monocytogenes ◽

Food Processing ◽

Benzalkonium Chloride ◽

Clinical Environment ◽

Outbreak Strain ◽

Content Type ◽

Chloride Resistance ◽

Processing Plants ◽

Hot Dog ◽

Widespread Dissemination

ABSTRACTAnalysis of a panel of 116Listeria monocytogenesstrains of diverse serotypes and sources (clinical, environment of food processing plants, and food) revealed that all but one of the 71 benzalkonium chloride-resistant (BCr) isolates harboredbcrABC, previously identified on a large plasmid (pLM80) of the 1998-1999 hot dog outbreak strain H7858. In contrast,bcrABCwas not detected among BC-susceptible (BCs) isolates. ThebcrABCsequences were highly conserved among strains of different serotypes, but variability was noted in sequences flankingbcrABC. The majority of the BCrisolates had either the pLM80-type of organization of thebcrABCregion or appeared to harborbcrABCon the chromosome, adjacent to novel sequences. Transcription ofbcrABCwas induced by BC (10 μg/ml) in strains of different serotypes and diversebcrABCregion organization. These findings reveal widespread dissemination ofbcrABCacross BCrL. monocytogenesstrains regardless of serotype and source, while also suggesting possible mechanisms ofbcrABCdissemination acrossL. monocytogenesgenomes.

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Comparative Phenotypic and Genotypic Analysis of Swiss and Finnish Listeria monocytogenes Isolates with Respect to Benzalkonium Chloride Resistance

Frontiers in Microbiology ◽

10.3389/fmicb.2017.00397 ◽

2017 ◽

Vol 8 ◽

Cited By ~ 18

Author(s):

Anja B. Meier ◽

Claudia Guldimann ◽

Annukka Markkula ◽

Anna Pöntinen ◽

Hannu Korkeala ◽

...

Keyword(s):

Listeria Monocytogenes ◽

Benzalkonium Chloride ◽

Chloride Resistance ◽

Genotypic Analysis

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Heavy-Metal and Benzalkonium Chloride Resistance of Listeria monocytogenes Isolates from the Environment of Turkey-Processing Plants

Applied and Environmental Microbiology ◽

10.1128/aem.02426-07 ◽

2008 ◽

Vol 74 (5) ◽

pp. 1464-1468 ◽

Cited By ~ 77

Author(s):

S. Mullapudi ◽

R. M. Siletzky ◽

S. Kathariou

Keyword(s):

Listeria Monocytogenes ◽

Quaternary Ammonium ◽

Food Processing ◽

Benzalkonium Chloride ◽

The United States ◽

Limited Information ◽

Chloride Resistance ◽

Processing Plants ◽

Serotype 1 ◽

Serotype 4B

ABSTRACT The resistance of Listeria monocytogenes to cadmium and arsenic has been used extensively for strain subtyping. However, limited information is available on the prevalence of such resistance among isolates from the environment of food-processing plants. In addition, it is not known whether the resistance of such isolates to heavy metals may correlate with resistance to quaternary ammonium compounds extensively used as disinfectants in the food-processing industry. In this study, we characterized 192 L. monocytogenes isolates (123 putative strains) from the environment of turkey-processing plants in the United States for resistance to cadmium and arsenic and to the quaternary ammonium disinfectant benzalkonium chloride (BC). Resistance to cadmium was significantly more prevalent among strains of serotypes 1/2a (or 3a) and 1/2b (or 3b) (83% and 74%, respectively) than among strains of the serotype 4b complex (19%). Resistance to BC was encountered among 60% and 51% of the serotype 1/2a (or 3a) and 1/2b (or 3b) strains, respectively, and among 7% of the strains of the serotype 4b complex. All BC-resistant strains were also resistant to cadmium, although the reverse was not always the case. In contrast, no correlation was found between BC resistance and resistance to arsenic, which overall was low (6%). Our findings suggest that the processing environment of turkey-processing plants may constitute a reservoir for L. monocytogenes harboring resistance to cadmium and to BC and raise the possibility of common genetic elements or mechanisms mediating resistance to quaternary ammonium disinfectants and to cadmium in L. monocytogenes.

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Genetic Characterization of Plasmid-Associated Benzalkonium Chloride Resistance Determinants in a Listeria monocytogenes Strain from the 1998-1999 Outbreak

Applied and Environmental Microbiology ◽

10.1128/aem.02056-10 ◽

2010 ◽

Vol 76 (24) ◽

pp. 8231-8238 ◽

Cited By ~ 106

Author(s):

Driss Elhanafi ◽

Vikrant Dutta ◽

Sophia Kathariou

Keyword(s):

Listeria Monocytogenes ◽

Food Processing ◽

Benzalkonium Chloride ◽

Genetic Basis ◽

Genetic Characterization ◽

Chloride Resistance ◽

Processing Plants ◽

Resistant Strains ◽

Ammonium Compounds

ABSTRACT Quaternary ammonium compounds such as benzalkonium chloride (BC) are widely used as disinfectants in both food processing and medical environments. BC-resistant strains of Listeria monocytogenes have been implicated in multistate outbreaks of listeriosis and have been frequently isolated from food processing plants. However, the genetic basis for BC resistance in L. monocytogenes remains poorly understood. In this study, we have characterized a plasmid (pLM80)-associated BC resistance cassette in L. monocytogenes H7550, a strain implicated in the 1998-1999 multistate outbreak involving contaminated hot dogs. The BC resistance cassette (bcrABC) restored resistance to BC (MIC, 40 μg/ml) in a plasmid-cured derivative of H7550. All three genes of the cassette were essential for imparting BC resistance. The transcription of H7550 BC resistance genes was increased under sublethal (10 μg/ml) BC exposure and was higher at reduced temperatures (4, 8, or 25°C) than at 37°C. The level of transcription was higher at 10 μg/ml than at 20 or 40 μg/ml. In silico analysis suggested that the BC resistance cassette was harbored by an IS1216 composite transposon along with other genes whose functions are yet to be determined. The findings from this study will further our understanding of the adaptations of this organism to disinfectants such as BC and may contribute to the elucidation of possible BC resistance dissemination in L. monocytogenes.

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Genetic Determinants of Peripheral Artery Disease

Circulation Research ◽

10.1161/circresaha.121.318327 ◽

2021 ◽

Vol 128 (12) ◽

pp. 1805-1817

Author(s):

Derek Klarin ◽

Philip S. Tsao ◽

Scott M. Damrauer

Keyword(s):

Peripheral Artery Disease ◽

Complex Disease ◽

Association Studies ◽

Whole Genome Sequencing Data ◽

Genome Wide Association Studies ◽

Sequencing Data ◽

Genetic Determinants ◽

Peripheral Artery ◽

Common Complex Disease ◽

Artery Disease

Peripheral artery disease—atherosclerosis of the abdominal aorta and lower extremity vascular bed—is a complex disease with both environmental and genetic determinants. Unmitigated disease is associated with major functional decline and can lead to chronic limb-threatening ischemia, amputation, and increased mortality. Over the last 10 years, major advances have been made in identifying the genetic basis of this common, complex disease. In this review, we provide an overview of the primary types of genetic analyses performed for peripheral artery disease, including heritability and linkage studies, and more recently biobank-based genome-wide association studies. Looking forward, we highlight areas of future study including efforts to identify causal peripheral artery disease genes, rare variant and structural variant analyses using whole-exome and whole-genome sequencing data, and the need to include individuals of diverse genetic ancestries.

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