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

Abstract

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.

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

“…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].…”

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

“…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.…”

“…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).…”

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

“…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.…”

“…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].…”