Prevalence, Potential Virulence, and Genetic Diversity of Listeria monocytogenes Isolates From Edible Mushrooms in Chinese Markets

Abstract

Listeria monocytogenes, an intracellular foodborne pathogen, is capable of causing listeriosis, such as meningitis, meningoencephalitis, and abortion. In recent years, the occurrence of Listeria monocytogenes in edible mushroom products has been reported in several countries. There are no guidelines for qualitative and quantitative detection of L. monocytogenes in mushroom products in China. Therefore, this study aimed to investigate the prevalence and contamination level of L. monocytogenes in edible mushrooms in Chinese markets and to determine the antibiotic resistance and sequence types (STs) of these isolates to provide data for risk assessments. Approximately 21.20% (141/665) of edible mushroom samples were positive for L. monocytogenes, while 57.44% (81/141) of positive samples contained contamination levels of less than 10 MPN/g. The 180 isolates derived from positive samples belonged to serogroup I.1 (1/2a-3a, n = 111), followed by serogroup II.2 (1/2b-3b-7, n = 66), and serogroup III (4a-4c, n = 3). Antibiotic susceptibility testing showed that over 95% of L. monocytogenes isolates were resistant to penicillin, ampicillin, oxacillin, and clindamycin, while over 90% were susceptible to 16 antibiotic agents, the mechanisms of resistance remain to be elucidated. According to multilocus sequencing typing, the 180 isolates represented 21 STs, one of which was identified for the first time. Interestingly, ST8 and ST87 were predominant in edible mushroom products, indicating that specific STs may have distinct ecological niches. Potential virulence profiles showed that most of the isolates contained full-length inlA genes, with novel premature stop codons found in isolate 2035-1LM (position 1380, TGG→TGA) and 3419-1LM (position 1474, CAG→TAG). Five isolates belonging to serogroup II.2 carried the llsX gene from Listeria pathogenicity island (LIPI)-3, present in ST224, ST3, and ST619; 53 (29.44%) harbored the ptsA gene from LIPI-4, presenting in ST3, ST5, ST87, ST310, ST1166, and ST619. Five potential hypervirulent isolates carrying all three of these virulence factors were identified, suggesting edible mushrooms may serve as possible transmission routes of potential hypervirulent L. monocytogenes, which may be of great public health concern to consumers. Based on our findings, the exploration of novel approaches to control L. monocytogenes contamination is necessary to ensure the microbiological safety of edible mushroom products.

Isolation, Potential Virulence, and Population Diversity of Listeria monocytogenes From Meat and Meat Products in China

“…Most positive samples (90.5%) had less than 10 MPN/g, and only 3.9% of the samples had above 110 MPN/g, which were mainly chicken samples. These results were consistent with those of studies in other countries such as Poland (Modzelewska-Kapitula and Maj-Sobotka, 2014), Brazil (Ristori et al, 2014), and Ireland (Khen et al, 2015); similar results were also reported in China for other food items (Chen et al, 2018a,b), suggesting low levels of L. monocytogenes contamination in fresh food products. The low number of L. monocytogenes in most samples could still be problematic; being psychrotrophic, it may grow during the storage period.…”

“…The llsX gene (listeriolysin S, representing LIPI-3), which encodes a haemolytic cytotoxic factor associated with the destruction of gut microbiota during infection, is mainly present in a subset of lineage I (Cotter et al, 2008; Quereda et al, 2017a,b). LIPI-3 has been detected in several sequence types (STs) of L. monocytogenes strains, including ST1, ST3, ST4, ST6, ST77, ST79, ST191, ST213, ST217, ST224, ST288, ST363, ST380, ST382, ST389, ST489, ST554, ST581, ST619, ST778, ST999, ST1000, and ST1001 (Chen et al, 2018b; Kim et al, 2018; Wang et al, 2018). Furthermore, a cellobiose-family phosphotransferase system with a cluster of six genes was recently identified as LIPI-4 (Maury et al, 2016).…”

Association between edible mushroom intake and the prevalence of newly diagnosed non-alcoholic fatty liver disease: results from the Tianjin Chronic Low-Grade Systemic Inflammation and Health Cohort Study in China

“…Many people in China consume a variety of edible mushrooms daily (28) . Mushrooms contain many nutritional components such as polyphenols, vitamins, minerals, fibres and polysaccharides (29) .…”

Occurrence, Antibiotic Resistance, and Population Diversity of Listeria monocytogenes Isolated From Fresh Aquatic Products in China

“…Eight isolates (11.11%) carried the llsX gene and mainly belonged to ST1, ST3, ST308, ST323, ST330, and ST619, whereas 15 isolates belonging to ST87 showed the presence of LIPI-4 in this study. LIPI-3 were mainly present in lineage I, included 21 STs belongs to 18 CCs (CC1, CC3, CC4, CC6, CC191, CC213, CC217, CC224, CC288, CC363, CC379, CC382 CC389, CC489, CC554, CC581, CC1000, and CC380) ( Chen et al, 2018 ; Hilliard et al, 2018 ; Kim et al, 2018 ; Wang et al, 2018 ). While LIPI-4 were only reported in CC4 isolates by Maury et al (2016) , recent studies reported that LIPI-4 presented in several other lineage I CCs and in a single lineage III CC in China, the United States, and Ireland, namely ST4, ST87, ST213, ST217, ST363, ST382, ST388, ST663, ST1002, ST1166, and ST619 ( Chen et al, 2018 ; Hilliard et al, 2018 ; Kim et al, 2018 ; Wang et al, 2018 ).…”

“… Maury et al (2016) identified that a cluster of six genes annotated as the cellobiose-family phosphotransferase system (PTS) and designated as LIPI-4, was highly associated with L. monocytogenes neuroinvasiveness and human maternal-neonatal (MN) infection. At present, LIPI-3 were found only in lineage I clonal complexes, 23 STs were found to carried LIPI-3 (ST1, ST1001, ST3, ST4, ST6, ST191, ST213, ST217, ST224, ST288, ST363, ST79, ST77, ST382, ST389, ST489, ST999, ST554, ST581, ST1000, ST380, ST778, and ST619), LIPI-4 presented in 11 STs belongs to lineage I and a single lineage III (ST4, ST87, ST213, ST217, ST363, ST382, ST388, ST663, ST1002, ST1166, and ST619) ( Chen et al, 2018 ; Kim et al, 2018 ; Wang et al, 2018 ). The presence of these virulence genes may be an important determinant to their pathogenicity.…”