1. Introduction
The current food trends caused by the COVID-19 pandemic have renewed the interest in healthy lifestyles motivating the consumption of healthy foods [1]. Fresh produce provides vitamins, minerals, and fibers [2]. Consumption of fresh vegetables is considered to prevent obesity, cardiovascular diseases, and osteoporosis [2,3]. However, leafy vegetables are among the foods most associated with disease outbreak [4]. The foodborne outbreaks are caused by contaminated vegetables and related pathogenic bacteria such as Bacillus cereus, Salmonella, and Escherichia coli O157:H7 [1,5]. Vegetables are often consumed directly or only with minimal processing that does not eliminate pathogenic bacteria [5]. Food poisoning outbreaks caused by food contaminated with B. cereus included 120 cases from 2003 to 2022 in Korea [6].
B. cereus is a gram-positive, spore-forming, facultative aerobe motile rod and an opportunistic human pathogen that belongs to the B. cereus species group [7,8,9]. This group consists of the eight species B. cereus, B. mycoides, B. pseudomycoides, B. thuringiensis, B. weihenstephanensis, B. anthracis, B. cytotoxicus, and B. toyonensis [9]. B. cereus causes food spoilage and food poisoning in humans [8]. Food poisoning caused by B. cereus is of two types: diarrheal and emetic. The diarrheal type is caused by the production of heat-labile enterotoxins produced during the vegetative growth of B. cereus in the small intestine, including hemolysin BL (HBL), non-hemolytic enterotoxin (NHE), single protein enterotoxin cytotoxin K, and enterotoxin FM, whereas the emetic type is caused by cereulide produced during the growth of B. cereus cells in food [9,10,11]. Foods often related to diarrheal food poisoning include meat products, soups, vegetables, sauces, and dairy products, while those related to the emetic food poisoning are mainly rice and pasta [12]. Some B. cereus strains cause hospital acquired infections; however, the occurrence of these infections caused by B. cereus is low, but the mortality is high, regardless of aggressive treatment with antibiotics [13]. B. cereus produces β-lactamases, and it is resistant to β-lactam antibiotics, including the third generation cephalosporins. However, B. cereus is susceptible to clindamycin, aminoglycosides, chloramphenicol, vancomycin, and erythromycin [14].
Garlic chives (Korean leek, Allium tuberosum Rottler) belong to the family Alliaceae and include garlic and onions, which are some of the most commonly used vegetable ingredients in Korean dishes [15]. Garlic chives are rich in nutrients such as vitamins, carbohydrates, minerals, and cellulose [16]. A study reported that the level of B. cereus contamination in garlic chives was 1.30 to 5.08 log CFU/g [17]. Since garlic chives are cultivated in contact with the soil, contaminated soil can cause cross-contamination with B. cereus in garlic chives [17].
The distribution of B. cereus in plants and cultivated environments has been reported in previous studies. However, the number of studies on plants and cultivated environments, especially composts and irrigation water, is insignificant. Additionally, there are few studies pertaining to the characteristics of the enterotoxin profile and antibiotic resistance of B. cereus isolated from cultivated environments. Therefore, the purpose of this study was to investigate the pattern of enterotoxin genes and antibiotic resistance of B. cereus isolated from garlic chives and agricultural environment including soil, compost, and irrigation water.
2. Materials and Methods
2.1. Bacterial Strains
Garlic chives and agricultural environment including soil, composts, and irrigation water were collected from garlic chive farms in Korea. B. cereus, which was isolated by MYP agar from samples, was collected and stocked in our previous study [18]. The β-hemolysis and groEL gene of B. cereus were identified using the blood agar culture method and polymerase chain reaction (PCR). In total, 13 garlic chive samples, 67 soil samples, 17 compost samples, and 6 irrigation water samples were studied in this study [18].
2.2. Detection of Enterotoxin Genes
The isolates were streaked on tryptic soy agar (TSA) and incubated at 28 °C for 18 to 24 h. The DNA templates were extracted using DNA extraction kit for the PCR assay. PCR amplification was conducted with a 20 μL reaction mixture consisting of AccuPower PCR premix (Bioneer, Daejeon, Korea), 20 to 50 ng of DNA template, and 10 pmol of each primer using a thermal cycler (C1000TM Thermal Cycler, BIO-RAD, CA, USA). The primer pairs used for amplifying the hblACD and nheABC genes were prepared as described by Park et al. [14]. Amplification reactions were performed as described by Park et al. [14] with modifications. The template DNA was preheated to 94 °C for 7 min. The hblA gene was amplified for 35 cycles of 45 s at 94 °C for denaturation, 45 s at 58 °C for annealing, and 45 s at 72 °C for extension, followed by a final extension at 72 °C for 7 min. The PCR conditions for the hblC and hblD genes consisted of 35 cycles of 30 s at 94 °C for denaturation, 30 s at 54 °C for annealing, and 30 s at 72 °C for extension. The PCR conditions for the nheA, nheB, and nheC genes consisted of 35 cycles of 30 s at 94 °C for denaturation, 30 s at 55 °C for annealing, and 30 s at 72 °C for extension. The PCR products were electrophoresed on a 2% agarose gel. B. cereus ATCC 14579 was used as the control.
2.3. Antibiotic Susceptibility Testing
Antibiotic susceptibility of B. cereus was evaluated according to the method described by the Clinical and Laboratory Standards Institute (CLSI) [19]. The antimicrobial agents tested and their concentrations were as follows: penicillin (10 U), oxacillin (1 μg), cefotaxime (30 μg), cefoxitin (30 μg), imipenem (10 μg), gentamicin (10 μg), streptomycin (10 μg), rifampicin (5 μg), trimethoprim-sulfamethoxazole (25 μg), vancomycin (30 μg), clindamycin (2 μg), erythromycin (15 μg), linezolid (30 μg), chloramphenicol (30 μg), tetracycline (30 μg), and ciprofloxacin (5 μg). The susceptibility of B. cereus to each antimicrobial agent was measured, and the results were interpreted in accordance with the criteria provided by the CLSI. Staphylococcus aureus ATCC 29213 was selected as the control organism.
3. Results and Discussion
3.1. Distribution of Enterotoxin Genes in B. cereus from Different Sources
Diverse patterns of enterotoxin gene distribution were identified in B. cereus isolated from garlic chives and agricultural environments. Garlic chives had 4 patterns, soil had 11 patterns, compost had 6 patterns, and irrigation water had 1 pattern (Table 1). HBL and NHE complexes (hblA + hblC + hblD and nheA + nheB + nheC) were 23.1% (pattern G1), HBL complex was 61.5% (pattern G2), and NHE complex was 15.4% (pattern G3, G4) in garlic chives. In soil, HBL and NHE complexes were 47.8% (pattern S1), HBL complex was 32.8% (pattern S2-4), and NHE complex was 9.0% (pattern S5, S8). B. cereus isolated from soil has one or two hemolytic enterotoxin genes and two non-hemolytic enterotoxin genes on four different patterns (10.0%) and exhibits hblCD genes on one pattern (1.5%). In compost, HBL and NHE complexes were 23.5% (pattern C1) and HBL complex was 47.1% (pattern C2). B. cereus isolated from irrigation water showed 100% of HBL and NHE complexes (pattern W1). B. cereus isolated from compost has two hemolytic enterotoxin genes and one or two non-hemolytic enterotoxin genes on two patterns (11.8%) and exhibits one or two non-hemolytic enterotoxin genes on two patterns (17.6%).
HBL, a three-component hemolysin, consisting of a binding component (B, hblA) and lytic components (L1&L2, hblD, and hblC) and exhibiting enterotoxin activity, has been purified and characterized [20]. HBL complex has maximal hemolytic and cytotoxic activities [7]. NHE is a pore-forming toxin consisting of two lytic elements, nheA and nheB, and the protein nheC [21]. Since HBL and NHE are tripartite toxins, in both cases the three components are necessary to produce the active toxin [22]. HBL and NHE are considered the main virulence factors of B. cereus [14]. B. cereus is found in the ground, dust, or on different foods. Virulence or enterotoxin gene has been isolated from foods, clinical, soil, and environment samples [23]. B. cereus isolated from green leaves or vegetables such as garlic chives, bell peppers, perilla leaf, and romaine lettuce had high detection rates of the hblACD and nheABC genes [14]. Amor et al. [24] reported that diverse patterns of enterotoxin distribution of B. cereus were detected from fresh-cut vegetables in Tunisia; 20% HBL complex, 60% hblC + hblD gene, and 100% NHE complex [24]. In the present results, B. cereus isolated from garlic chives had 7.7% of hblC + hblD gene and 38.5% of NHE complex. A previous study [25] reported that B. cereus s.l. isolated from fresh vegetable samples such as cucumbers, carrots, herbs, salad leaves, and ready-to-eat mixed salads had various patterns; 91.2% hblDA, 73.5% nheAB, and 53.7% hblDA + nheAB complex. B. cereus strains isolated from Mexican chili powder were found to be positive for the hblC and nheA genes [26]. However, in the present study, 100, 92.3, 38.5, and 7.7% of B. cereus isolates from garlic chives were positive for hblD, hblC, nheA, and hblDA + nheABC complex (Table 1). Senesi and Ghelardi [12] reported that HBL was secreted by approximately 43% and NHE was produced by almost 100% of B. cereus strains isolated from environment and/or food. However, our study demonstrated that B. cereus isolated from garlic chives, soil, compost, and irrigation water secreted 80.6% the HBL complex and 51.5% NHE complex.
3.2. Antibiotic Susceptibility of B. cereus
The antibiotic resistance of B. cereus isolates to diverse antimicrobial agents is shown in Figure 1. Overall, B. cereus isolates were resistant to penicillin, oxacillin, cefotaxime, and cefoxitin, but were susceptible to imipenem. One isolate from garlic chives showed intermediate resistance to cefoxitin (Figure 1a). Two isolates from soil were susceptible to penicillin, oxacillin, and cefoxitin, and 10 isolates from soil had intermediate resistance to cefotaxime (Figure 1b). Six isolates from compost and one isolate from irrigation water possessed intermediate resistance to cefotaxime (Figure 1c,d). B. cereus isolated from garlic chives, soil, compost, and irrigation water was susceptible to non-β-lactam antibiotics, including gentamicin, streptomycin, rifampin, trimethoprim-sulfamethoxazole, vancomycin, clindamycin, erythromycin, linezolid, chloramphenicol, tetracycline, and ciprofloxacin. However, some isolates had intermediate resistance to antimicrobial agents such as rifampin, clindamycin, erythromycin, and tetracycline. Furthermore, B. cereus isolated from garlic chives showed intermediate resistance to rifampin (15.4%), clindamycin (30.8%), erythromycin (7.7%), and tetracycline (7.7%) (Figure 1a). B. cereus isolated from soil showed intermediate resistance to rifampin (17.9%), clindamycin (10.4%), erythromycin (6%), and tetracycline (3%) (Figure 1b). B. cereus isolated from compost had intermediate resistance to rifampin (5.9%), clindamycin (11.8%), and tetracycline (5.9%) (Figure 1c). B. cereus from irrigation water had intermediate resistance to rifampin (16.7%), clindamycin (33.3%), and tetracycline (33.3%) (Figure 1d). B. cereus ATCC 14579 showed resistance to penicillin, oxacillin, and cefoxitin, intermediate resistance to cefotaxime and rifampin, and susceptibility to 11 antibiotics.
A previous study reported that B. cereus strains isolated from raw vegetables such as garlic chives, bell peppers, perilla leaf, and romaine lettuce exhibited resistance to penicillin, cefotaxime, tetracycline, clindamycin, and rifampin [14]. B. cereus strains isolated from perilla leaf showed resistance to penicillin, resistance and susceptibility to oxacillin, resistance, intermediate resistance, and susceptibility to rifampin, and susceptibility to imipenem [27]. B. cereus isolated from clinical patients and foods, including dairy products, salad, rice, and infant food, had resistance to some glycopeptides, aminoglycosides, tetracycline, and carbapenems [28]. Our results were consistent with the patterns reported in previous studies. We found that B. cereus isolated from garlic chives exhibited the resistance against penicillin, oxacillin, and cefotaxime, the intermediate resistance against rifampin, clindamycin, and tetracycline, and susceptibility to imipenem. However, the pattern of tetracycline observed in our study (intermediate resistance and susceptibility) differed from that reported previously. Jensen et al. [29] reported that B. cereus group isolated from farm soil had penicillin, erythromycin, and streptomycin resistance. However, in our study, B. cereus isolated from soil showed resistance to penicillin, intermediate resistance to erythromycin, and susceptibility to streptomycin and erythromycin. B. cereus produces β-lactamase and is resistant to β-lactam antibiotics including third generation cephalosporins [13]. Most B. cereus isolates in this study showed resistance to penicillin, oxacillin, cefotaxime, and cefoxitin. It has been reported that B. cereus isolated from grassland soil was resistant to penicillin, sulbactam+ampicillin, trimethoprim-sulfamethoxazole, and oxacillin [30]. B. cereus is generally susceptible to clindamycin, aminoglycosides, chloramphenicol, vancomycin, and erythromycin [31]. Luna et al. [32] reported that B. cereus isolated from the environment and soil showed intermediate resistance or resistance to clindamycin and resistance to erythromycin. The variations in antibiotic resistance profiles observed in this study can be explained by the fact that environmental conditions can induce stress in bacteria, thereby impacting bacterial susceptibility to antimicrobials [33]. When bacteria are exposed to environmental stress, they may undergo genotypic and phenotypic changes, which may subsequently change their antibiotic resistance profiles [13].
4. Conclusions
The present study revealed the various pattern of enterotoxin profiles in B. cereus isolated from garlic chives and the agricultural environment (soil, compost, and irrigation water) in Korea. B. cereus isolates had resistance to penicillin, oxacillin, cefotaxime, and cefoxitin, and intermediate resistance to cefotaxime, rifampin, clindamycin, erythromycin. The results of the present study indicate the potential of B. cereus in garlic chives and the agricultural environment to cause diarrhea syndrome. Additionally, B. cereus strains exhibited multidrug resistance and the diversity of antibiotic resistance profiles showed that it changed from susceptibility to intermediate resistance or resistance to intermediate resistance and susceptibility. Therefore, it needs the intensive monitoring of garlic chives and agricultural environment to protect consumer health from food poisoning and antibiotic multi-resistance.
Investigation and writing—original draft preparation, J.J.; investigation, H.J., S.S., M.J. and B.K.; writing—review, K.R.; supervision, K.O. All authors have read and agreed to the published version of the manuscript.
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The authors declare no conflict of interest.
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Enlarge this image.Figure 1. Antibiotic susceptibility of B. cereus isolated from garlic chives (a), soil (b), compost (c), and irrigation water (d) was determined by disk diffusion method. P, penicillin; OX, oxacillin; CTX, cefotaxime; FOX, cefoxitin; IPM, imipenem; CN, gentamicin; S, streptomycin; RD, rifampin; SXT, trimethoprim-sulfamethoxazole; VA, vancomycin; DA, clindamycin; E, erythromycin; LZD, linezolid; C, chloramphenicol; TE, tetracycline; CIP, ciprofloxacin.
B. cereus isolated from garlic chives and environment had diverse patterns of enterotoxin genes distributions.
| Sample | No. of Isolates (%) | Toxin Genes | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Pattern | hblA | hblC | hblD | hblACD 1 | nheA | nheB | nheC | nheABC 2 | ||
| Garlic chives | 3/13 (23.1) | G1 | + | + | + | + | + | + | + | + |
| 8/13 (61.5) | G2 | + | + | + | + | — | + | + | — | |
| 1/13 (7.7) | G3 | + | — | + | — | + | + | + | + | |
| 1/13 (7.7) | G4 | — | + | + | — | + | + | + | + | |
| Soil | 32/67 (47.8) | S1 | + | + | + | + | + | + | + | + |
| 7/67 (10.4) | S2 | + | + | + | + | + | — | + | — | |
| 3/67 (4.5) | S3 | + | + | + | + | + | — | — | — | |
| 12/67 (17.9) | S4 | + | + | + | + | — | + | + | — | |
| 5/67 (7.5) | S5 | + | — | + | — | + | + | + | + | |
| 1/67 (1.5) | S6 | + | — | + | — | + | + | — | — | |
| 2/67 (3.0) | S7 | + | — | + | — | — | + | + | — | |
| 1/67 (1.5) | S8 | — | + | + | — | + | + | + | + | |
| 2/67 (3.0) | S9 | — | + | + | — | + | — | + | — | |
| 1/67 (1.5) | S10 | — | + | + | — | — | — | — | — | |
| 1/67 (1.5) | S11 | — | — | + | — | + | — | + | — | |
| Compost | 4/17 (23.5) | C1 | + | + | + | + | + | + | + | + |
| 8/17 (47.1) | C2 | + | + | + | + | — | + | + | — | |
| 1/17 (5.9) | C3 | + | — | + | — | + | — | — | — | |
| 1/17 (5.9) | C4 | — | + | + | — | + | — | + | — | |
| 2/17 (11.8) | C5 | — | — | — | — | + | — | + | — | |
| 1/17 (5.9) | C6 | — | — | — | — | — | — | + | — | |
| Irrigation water | 6/6 (100.0) | W1 | + | + | + | + | + | + | + | + |
1 hblACD, hblA + hblC + hblD. 2 nheABC, nheA + nheB + nheC.
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; Jin, Hyeonsuk 2 ; Seo, Seungmi 2 ; Jeong, Myeongin 2 ; Kim, Boeun 2 ; Ryu, Kyoungyul 2 ; Oh, Kwangkyo 2 1 Functional Food Division, Department of Agro-Food Resources, National Institute of Agricultural Sciences, Rural Development Administration, Wanju-gun 55365, Jeolloabuk-do, Korea
2 Microbial Safety Division, Department of Agro-food Safety and Crop Protection, National Institute of Agricultural Sciences, Rural Development Administration, Wanju-gun 55365, Jeollabuk-do, Korea