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Characterization of Clostridium Novyi Isolated from a Sow in a Sudden Death Case in Korea

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Characterization of Clostridium Novyi Isolated from a Sow in a Sudden Death Case in Korea Jeong et al. BMC Veterinary Research (2020) 16:127 https://doi.org/10.1186/s12917-020-02349-9 RESEARCH ARTICLE Open Access Characterization of Clostridium novyi isolated from a sow in a sudden death case in Korea Chang-Gi Jeong1, Byoung-Joo Seo1, Salik Nazki1, Byung Kwon Jung2, Amina Khatun1,3, Myeon-Sik Yang1, Seung-Chai Kim1, Sang-Hyun Noh4, Jae-Ho Shin2, Bumseok Kim1 and Won-Il Kim1* Abstract Background: Multifocal spherical nonstaining cavities and gram-positive, rod-shaped, and endospore-forming bacteria were found in the liver of a sow that died suddenly. Clostridium novyi type B was identified and isolated from the sudden death case, and the isolate was characterized by molecular analyses and bioassays in the current study. Results: C. novyi was isolated from the liver of a sow that died suddenly and was confirmed as C. novyi type B by differential PCR. The C. novyi isolate fermented glucose and maltose and demonstrated lecithinase activity, and the cell-free culture supernatant of the C. novyi isolate exhibited cytotoxicity toward Vero cells, demonstrating that the isolate produces toxins. In addition, whole-genome sequencing of the C. novyi isolate was performed, and the complete sequences of the chromosome (2.29 Mbp) and two plasmids (134 and 68 kbp) were identified for the first time. Based on genome annotation, 7 genes were identified as glycosyltransferases, which are known as alpha toxins; 23 genes were found to be related to sporulation; 12 genes were found to be related to germination; and 20 genes were found to be related to chemotaxis. Conclusion: C. novyi type B was isolated from a sow in a sudden death case and confirmed by biochemical and molecular characterization. Various virulence-associated genes were identified for the first time based on whole- genome sequencing. Keywords: Anaerobe, Clostridium novyi, Isolation, Characterization, Whole-genome sequencing Background Based on the toxins they produce, C. novyi are classi- Clostridium novyi (C. novyi), originally named Bacillus fied into four types: A, B, C and D. C. novyi type A pro- oedematis maligni no. 2, was first isolated in 1894 from duces alpha, gamma, delta and epsilon toxins. C. novyi guinea pigs by Dr. Frederick Novy [1]. C. novyi is broadly type B produces alpha, beta, and zeta toxins, while type distributed in soil, water and marine sediments and affects C produces gamma toxin [2, 6, 7]. C. novyi type D is humans and animals worldwide [2–4]. C. novyi is a gram- considered to be a different species, Clostridium haemo- positive, noncapsulated, motile obligatory anaerobe that pro- lyticum, because it does not produce alpha toxin and be- duces endospores to resist unfavorable environments [1, 5]. cause the disease that it causes is different from those caused by types A and B [8]. C. haemolyticum produces beta, eta and theta toxins [9]. C. novyi type A is fre- * Correspondence: [email protected] quently involved in gas gangrene infections in humans 1College of Veterinary Medicine, Jeonbuk National University, 79 Gobong-ro, Iksan, Jeonbuk 54596, Republic of Korea and animals, while type B is the etiological agent of Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Jeong et al. BMC Veterinary Research (2020) 16:127 Page 2 of 9 infectious necrotic hepatitis (black disease), which is typic- exhibits beta hemolysis on blood agar. The biochemical ally observed in sheep, cattle and swine [10]. C. novyi type characteristics of the C. novyi isolate are summarized in C is not known to induce illness in and is typically consid- Table 1. The C. novyi isolate was positive for D-glucose, ered nonpathogenic toward laboratory animals [7]. C. gelatin, D-maltose, salicin, L-rhamnose, D-cellobiose, novyi type D (C. haemolyticum) is responsible for and lecithinase and negative for L-tryptophan, urea, D- hemoglobinuria in calves [7], while C. novyi types A and B mannitol, D-lactose, D-saccharose, D-xylose, L- (producing alpha toxin) cause sudden death in swine, and arabinose, esculin, glycerol, D-mannose, D-melezitose, the carcasses exhibit gross distension and livers with gas D-sorbitol, D-trehalose, and catalase. bubble infiltration or sponge-like appearances [11, 12]. The 16S rRNA gene sequence has been used to detect Phylogenetic analysis of the isolate based on the 16S genetic relatedness between different species of bacteria. rRNA gene sequence Currently, next-generation sequencing is utilized as a Based on the 16S rRNA gene sequence analysis, the C. rapid tool to perform whole-genome sequencing of clin- novyi isolate showed more than 99% similarity with C. ical isolates. Indeed, this method has proved to be of novyi types B and C, C. haemolyticum, and C. botulinum great value for understanding bacterial evolution, out- types C and D. The C. novyi isolate exhibited 84 to 91% breaks, toxigenicity, and antimicrobial resistance in a similarity with C. perfringens, C. sporogenes,andC. sor- number of studies involving Vibrio cholera, Escherichia dellii. A comparison of the 16S rRNA gene sequences of coli, Clostridium difficile, and Mycobacterium tubercu- the C. novyi isolate with those of different Clostridium losis [12, 13]. In the present study, for the first time, C. species is shown in Fig. 2. novyi type B was isolated from a sudden death case of a sow in Korea, and the isolate was characterized by mo- Histopathological examination of the liver lecular analyses and bioassays. To the best of our know- The liver tissues showed coagulative necrosis throughout ledge, this is the first report of the complete genome the entire field. Multifocal spherical nonstaining cavities sequence of C. novyi type B in Korea. were found that were well demarcated, and the cavity margins were clear (Fig. 3a and b) Furthermore, gram- Results positive, rod-shaped bacteria were observed on the liver Isolation of the C. novyi isolate tissue (Fig. 3c). After 72 h of anaerobic incubation, colonies showing ir- regular shapes with unclear borders appeared on agar Cell culture assay of the C. novyi isolate on Vero cells media, and gram-positive, rod-shaped, endospore- The cell-free supernatant of C. novyi reference strains, forming bacteria were identified in the colonies (Fig. 1a ATCC 17861 (C. novyi type A) and ATCC 25758 (C. and b). Differential PCR was conducted on the DNA ex- novyi type B) were tested on Vero 76 cells that were ob- tracted from a single colony, which confirmed the isolate served for 5 days. Abnormal cells were detected in all of as C. novyi type B [14]. No other bacterial and viral the strains at days 1 and 2 for the 1:4 and 1:8 dilutions, pathogens were detected (data not shown). respectively. On day 3, rounding and retracting cells were observed up to dilutions of 1:32 from inoculation Biochemical characterization of the C. novyi isolate of cell-free supernatants of ATCC 17861 and ATCC Biochemical analysis revealed that the C. novyi isolate 25758, while the cell-free supernatant of the C. novyi generates gas when treated with hydrogen peroxide and isolate (150775) showed abnormal cells up to dilutions Fig. 1 Morphology of the Clostridium isolate based on staining. a Gram staining was performed on the cultured isolate, resulting in the detection of gram-positive rods. b Endospores of the cultured C. novyi isolate were observed after staining with 5% malachite green Jeong et al. BMC Veterinary Research (2020) 16:127 Page 3 of 9 Table 1 Biochemical test results for the C. novyi isolate (accession numbers: CP029458.1, CP029459.1, and Active ingredients Results CP029460.1). D-Glucose + Gelatin + Prediction of genes associated with pathogenicity All of the identified genes of the C. novyi isolate are Lecithinase + summarized in Additional file 1. A total of 35 genes – L-Tryptophan related to sporulation and germination were detected in Urea – the whole genome of the C. novyi isolate. Among these D-Mannitol – genes, sporulation-related sigma factors (DFH04_ D-Lactose – RS02880, DFH04_RS08440, DFH04_RS08465, DFH04_ D-Saccharose + RS08470, and DFH04_RS10365) and stage-specific sporulation genes were detected. Additionally, 7 D-Maltose + glycosyltransferase genes associated with the Salicin + monoglycosyltransferase activity of alpha toxin were D-Xylose – identified (DFH04_RS05070, DFH04_RS05155, DFH04_ L-Arabinose – RS10400, DFH04_RS10410, DFH04_RS10425, DFH04_ Esculin – RS10435, and DFH04_RS10440). Various genes encoding Glycerol – chemotaxis proteins were also identified in the C. novyi isolate genome, including a sensor kinase, the D-Cellobiose + product of DFH04_RS10060; a deamidase, the product – D-Mannose of DFH04_RS08070; a methyltransferase, the product D-Melezitose – of DFH04_RS10065; a docking protein, the product of D-Sorbitol – DFH04_RS08070; and a phosphatase protein, the L-Rhamnose + product of DFH04_RS10055. Additionally, 9 genes D-Trehalose – were identified as methyl-accepting chemotaxis pro- teins (MCPs).
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