Coselection of Cadmium and Benzalkonium Chloride Resistance in Conjugative Transfers from Nonpathogenic Listeria spp. to Other Listeriae

Katharios-Lanwermeyer, Stefan; Rakić-Martinez, Mira; Elhanafi, Driss; Ratani, Shakir; Tiedje, James M.; Kathariou, Sophia

doi:10.1128/aem.02245-12

Cited by 67 publications

(57 citation statements)

References 53 publications

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“…Additional sequencing will be also needed to elucidate the genomic locations of bcrABC in strains of other categories (including category VI isolates that appear to harbor bcrABC on the chromosome). Furthermore, it will be of interest to characterize the bcrABCharboring regions of nonpathogenic Listeria spp., which may serve as reservoirs for bcrABC and other resistance determinants for L. monocytogenes (25).…”

Section: Resultsmentioning

confidence: 99%

“…Strains showing confluent growth of the spots upon exposure to BC (10 g/ml) were considered resistant (23). For MIC determinations, a single colony from a blood agar plate (Remel) was resuspended in 100 l of Mueller-Hinton broth (BD), 5 l of the suspension was spotted in duplicate on Mueller-Hinton agar with variable concentrations of BC (0, 5,10,15,20,25,30,35, and 40 g/ml), and the plates were incubated at 25°C for 48 h. The MIC was defined as the lowest assessed concentration of BC that prevented confluent growth of the spots. MICs were determined in at least two independent trials.…”

Section: Methodsmentioning

confidence: 99%

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Conservation and Distribution of the Benzalkonium Chloride Resistance Cassette bcrABC in Listeria monocytogenes

Dutta

Elhanafi

Kathariou

2013

Appl Environ Microbiol

103

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bAnalysis of a panel of 116 Listeria monocytogenes strains of diverse serotypes and sources (clinical, environment of food processing plants, and food) revealed that all but one of the 71 benzalkonium chloride-resistant (BC r ) isolates harbored bcrABC, previously identified on a large plasmid (pLM80) of the 1998-1999 hot dog outbreak strain H7858. In contrast, bcrABC was not detected among BC-susceptible (BC s ) isolates. The bcrABC sequences were highly conserved among strains of different serotypes, but variability was noted in sequences flanking bcrABC. The majority of the BC r isolates had either the pLM80-type of organization of the bcrABC region or appeared to harbor bcrABC on the chromosome, adjacent to novel sequences. Transcription of bcrABC was induced by BC (10 g/ml) in strains of different serotypes and diverse bcrABC region organization. These findings reveal widespread dissemination of bcrABC across BC r L. monocytogenes strains regardless of serotype and source, while also suggesting possible mechanisms of bcrABC dissemination across L. monocytogenes genomes. Listeria monocytogenes is a food-borne pathogen that can cause severe illness and death in susceptible individuals (pregnant women and their fetuses, the elderly, and patients with various types of immunosuppression) (1, 2). An array of adaptations, including biofilm formation, cold tolerance, and resistance to disinfectants and to phage, can contribute to the ability of this pathogen to persist in food processing environments and thus contaminate ready-to-eat products (3-8). However, our understanding of the mechanisms and factors affecting such adaptations remains limited.Quaternary ammonium compounds such as benzalkonium chloride (BC) are extensively used in food processing and health care environments (9, 10). BC resistance has been detected in L. monocytogenes strains of different serotypes and from diverse sources (11)(12)(13)(14). Characterization of L. monocytogenes from foods and food processing plants revealed that most BC-resistant (BC r ) isolates were also resistant to the heavy metal cadmium, although the reverse was not always the case (14). Two distinct cadmium resistance determinants (cadA1 and cadA2) were identified among these BC r isolates, alone or together (14, 15). Of these, cadA1 is harbored on Tn5422, associated with plasmids of various sizes (16-18), whereas cadA2 has been identified on large plasmids, such as pLM80 of L. monocytogenes H7858, implicated in the 1998-1999 hot dog-associated outbreak of listeriosis, and pLI100 of L. innocua CLIP 11262 (17,19,20).In pLM80 of L. monocytogenes H7858, cadA2 appears to be a component of a composite transposon flanked by IS1216 elements (IS1216 left and IS1216 center in Fig. 1A). In the vicinity of cadA2 a three-gene cassette (bcrABC) was found to be associated with resistance to quaternary ammonium disinfectants such as BC. This cassette also appears to be a component of two putative transposable units, one flanked by IS1216 center and IS1216 right and the other flanked by ...

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Conservation and Distribution of the Benzalkonium Chloride Resistance Cassette bcrABC in Listeria monocytogenes

Dutta

Elhanafi

Kathariou

2013

Appl Environ Microbiol

103

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“…Even though these isolates grew poorly or not at all at the previous resistance threshold of 70 g/ml (11,15,23), they grew well at 35 g/ml. In contrast, other cadmium-susceptible isolates of L. monocytogenes typically have a cadmium MIC of 10 g/ml (24). All other cadmium-resistant isolates had MICs of Ն140 g/ml, regardless of their clonal group or determinant type ( Table 1).…”

mentioning

confidence: 99%

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

Lee

Rakić-Martinez

Graves

et al. 2013

Appl Environ Microbiol

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cIn Listeria monocytogenes serotype 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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“…Co-selection between cadmium resistance and BC resistance has not been documented before Since all BC-resistant strains were also resistant to cadmium, cadmium resistance may have been co-selected upon exposure to BC, as observed during in vitro conjugative transfers (117). However, we also identified strains that were cadmium-resistant but BC-susceptible.…”

Section: Assessment Of Othermentioning

confidence: 70%

“…Listeria (104,105,168,197). We recently provided evidence suggesting that non-pathogenic Listeriae may constitute reservoirs for resistance to the quaternary ammonium disinfectant benzalkonium chloride (BC), being able to conjugatively disseminate resistance to BC to other Listeriae, including L. monocytogenes (117). Cadmium resistance that was also exhibited by the BC-resistant non-pathogenic strains was found to be a useful marker for assessing transfer potential, and cadmium-resistant transconjugants harbored the corresponding resistance determinant (cadA1 or cadA2) (117).…”

Section: Such Findings Suggest the Need To Characterize Horizontal Trmentioning

confidence: 99%

Identification of the mechanisms of resistance and potential cross resistance of Listeria monocytogenes upon adaptation to different antimicrobials

Rakić-Martinez¹

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ACKNOWLEDGMENTSI would like to thank Dr. Vera Katić for being my mentor, not only through PhD studies, but in my undergraduate years as well. Her objectivity, articulate thinking and dedication to work inspired me to keep moving forward even after long, tiresome days in the lab. I will forever appreciate Dr. Katic's encouragement to pursue personal happiness and her support in important life decisions.I am forever grateful to Dr. Sophia Kathariou for accepting me in her lab and making me feel at home while far from it. Her incredible ability to find the best solutions when things were not looking promising and open completely new horizons along with her creativity and knowledge made science so attractive. Looking at all the great, bright and skilful young people pursuing their dreams under Dr. Kathariou's guidance makes me very proud for being a part of it.My appreciation also goes to Dr. Lepšanović and Dr. Mišić for accepting to be members of the committee. I am thankful to all my lab mates and to Ms. Robin Siletzky for her solid support throughout my work. A special thanks to Dr. Vikrant Dutta for his patience, willingness to help and his much admired teaching skills.Lastly and foremost I would like to thank my family. To my dear parents Ljubo and Zora whose unconditional love, support and presence whenever I needed them have been and will always be my motive to be better. To my big brother Zoran, who has been, and is my role model, but still owes me German lessons. Finally, I want to thank my boys, my beloved husband Sergio and my precious son Gregory, who have been an endless source of energy, support and love. Thanks for being my wingmen guys! ABSTRACTAbility to contaminate ready-to-eat, highly processed, cold-stored food products, relatively high fatality rate and environmental adaptations define .Listeria monocytogenes as a challenging foodborne pathogen of high public health significance. Listeria's adaptations and prolonged persistence in food processing facilities are a key link to contamination of foods.In recent years, bacterial multidrug resistance has been recognized as an emerging health challenge. Exposure to antimicrobials (antibiotics, disinfectants or environmentally ubiquitous heavy metals), may provide selective pressures for resistance with accompanying cross-resistance and increase in environmental fitness.In this work I addressed some of the possible mechanisms of adaptations that may contribute to persistence of L. monocytogenes in the environment as well as to survival and growth in different foods. This includes adaptations to heavy metals such as cadmium, disinfectants such as benzalkonium chloride (BC), selected antibiotics (e.g. the fluoroquinolone ciprofloxacin) and other toxic compounds (e.g. tetraphenyl-phosponium, often used as an anti-carcinogenic and efflux pump substrate). In order to characterize the impact of multidrug resistance on survival and growth of L. monocytogenes in different foods, we tested mutants adapted to higher concentrations of antibiotic ciprofloxacin and ...

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Coselection of Cadmium and Benzalkonium Chloride Resistance in Conjugative Transfers from Nonpathogenic Listeria spp. to Other Listeriae

Cited by 67 publications

References 53 publications

Conservation and Distribution of the Benzalkonium Chloride Resistance Cassette bcrABC in Listeria monocytogenes

Conservation and Distribution of the Benzalkonium Chloride Resistance Cassette bcrABC in Listeria monocytogenes

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

Identification of the mechanisms of resistance and potential cross resistance of Listeria monocytogenes upon adaptation to different antimicrobials

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