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Molecular Identification and Pathogenicity of Citrobacter And Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx Contents lists available at ScienceDirect Egyptian Journal of Aquatic Research journal homepage: www.sciencedirect.com/locate/ejar Full length article Molecular identification and pathogenicity of Citrobacter and Serratia species isolated from cultured Oreochromis niloticus ⇑ Manal I. El-Barbary a, , Ahmed M. Hal b a Fish Diseases Lab, National Institute of Oceanography and Fisheries, Egypt b Genetics and Genetic Engineering Lab, National Institute of Oceanography and Fisheries, Egypt article info abstract Article history: This study aimed to isolate and characterize some pathogenic bacterial strains belonging to the family Received 5 August 2017 Enterobacteriaceae. They had been isolated from gills, liver, kidney and skin of naturally infected Revised 19 September 2017 Oreochromis niloticus and had been identified by biochemical test and 16S rRNA gene using four universal Accepted 25 September 2017 primers. Additionally, the isolates were tested for antimicrobial susceptibility, histopathological alter- Available online xxxx ations of liver, kidney and gills and the pathogenicity of the identified isolates for O. niloticus. The results of phylogenetic analysis placed the isolates in the family Enterobacteriaceae (genera Serratia and Keywords: Citrobacter) based on 99% homology. The primer pair (17F and 1390R) is the most appropriate pair of uni- Citrobacter sp. versal primers employed for the identification of 16S rRNA gene as a reason behind fish disease in Serbia Serratia sp. Phylogenetic analysis it covers as much as possible of the variable regions (Vs). V1 and V2 regions of 16S rRNA gene presented Histology weak evidence of the diversity of the genera Serratia. The mortality rate was 40–60% after challenging O. Antibiotic sensitivity niloticus by identified isolates, which revealed its sensitivity to ciprofloxacin and norfloxacin. Histological Oreochromis niloticus changes showed dilation in sinusoids with severe vacuolar degeneration in the liver, tubular degenera- tion and hemorrhage between renal tubules with pyknotic nuclei in the kidney, epithelial hyperplasia, aneurism and evident epithelium interstitial edema in gills of O. niloticus. This study concluded that these isolates should be considered as an opportunistic pathogen of O. niloticus. The study also states that the sequencing of 16S rRNA is an important tool for the identification of unknown bacterial species of fish pathogen. Ó 2017 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Introduction tilapia and mullet (Hassan et al., 2012). While, the first report of pathogenicity of Citrobacter braakii in fish was in Bursa (Altun Bacteriosis in fish has a worldwide distribution that causes et al., 2013). On the other hand, Serratia marcescens has been asso- either rapid or low mortality in an acute or chronic form (Baeck ciated with bacterial septicemias and mortalities in salmonids and et al., 2009; Austin et al., 1992). Bacterial Enterobacteriaceae has were recognized as emerging pathogens (Austin and Gibb, 1993). It been reported as an opportunistic pathogen in fish and has been is a common microorganism present in soil and fresh water. It is considered a marker of sewage pollution (Rajasekaran, 2008). classified as a proteobacteria that produces biosurfactant which Serratia and Citrobacter are bacterial genera belonging to the contributes to the pathogenesis (Horng et al., 2002) where several Enterobacteriaceae family, where Citrobacter freundii is one of the virulence factors were found within the genome of S. marcescens infectious agents that have been recognized as an opportunistic which were isolated from infected tilapia (Chan et al., 2013). pathogen in veterinary and medical sciences (Chuang et al., Numerous studies used nucleic acid-based methods to identify 2006); it was first mentioned as an emerging fish pathogen from the fish pathogenic bacteria (Buller, 2004), such as the 16S rRNA sunfish (Mola mola) in Japan (Sato et al., 1982). Jeremic et al. gene in which its value lies in slow evolution (Page and Holmes, (2003) recorded the first confirmation of C. freundii as a reason 1998). In addition, 16S rRNA contains a variable of highly behind fish disease in Serbia and also in Egypt. It was isolated from conserved regions that can be specific to a genus (Buller, 2004), therefore, 16S rRNA gene sequencing is a strong technique for mea- suring the genetic diversity of biological samples and microbial Peer review under responsibility of National Institute of Oceanography and taxonomy (Van Berkum et al., 2003). Of the primers described as Fisheries. ⇑ Corresponding author. common, many with the analysis of 16S rDNA sequence have been E-mail address: [email protected] (M.I. El-Barbary). used to elucidate prokaryotic biodiversity (Baker et al., 1999). https://doi.org/10.1016/j.ejar.2017.09.004 1687-4285/Ó 2017 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: El-Barbary, M.I., Hal, A.M. Molecular identification and pathogenicity of Citrobacter and Serratia species isolated from cultured Oreochromis niloticus. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.09.004 2 M.I. El-Barbary, A.M. Hal / Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx Based on different parts of 16S rRNA gene, recombination events bacterial DNA template and was filled up to 50 lL of PCR grade among species may sometimes cause a few incoherencies among water. The PCR started with a denaturation at 95 °C for 1 min fol- phylogenies (Young and Haukka, 1996), so longer sequences of lowed by 35 cycles of denaturation at 95 °C for 40 s, annealing at 16S rRNA give more accurate results concerning the classification 58 °C for 1 min and elongation at 72 °C for 2 min. Finally, the PCR of a new species. Citrobacter freundii isolated from tilapia finger- was extended for an additional 10 min at 72 °C (BioRad, T100 Ther- lings, showed symptoms such as tail necrosis and hemorrhage on mal Cycler). The results of amplification were analyzed on a 1.2% the skin (Thanigaivel et al., 2015). In addition, C. freundii caused agarose gel stained with ethidium bromide. PCR products were systemic hemorrhages and gastroenteritis in a number of different purified with a QiaQuick PCR purification kit (QIAGEN) and were fish (Austin et al., 1992; Sato et al., 1982). Histological changes in directly sent to Macrogen Inc. for sequencing of 16S rRNA using fish infected by C. freundii were recorded in rainbow trout fry, high throughput Applied Biosystems 3730XL sequencer. cyprinids and Catfish (Jeremic et al., 2003; Pádua et al., 2014). In Egypt, the studies of effects of C. freundii, C. braakii and S. marces- Phylogenetic analysis cens on fish are rare. The aims of this study were characterize and diagnose the bacterial strains of Citrobacter and Serratia species To find related species, the sequences obtained in this study isolated from O. niloticus based on the sequence of 16S rRNA gene were compared to those in the BLASTN database (http://www. as well as to study the mismatching rates of 4 universal primers ncbi.nlm.nih.gov/blast). The 16S rRNA genes of 24 related species and the variance of different regions of 16S rDNA gene of these iso- were used from the GenBank database to generate a phylogenetic lates. Also, antimicrobial susceptibility and pathogenicity of iso- tree. Their accession numbers are shown in (Fig. 1) and were con- lates and their histopathological alterations on liver, kidney and ducted in MEGA6 (Tamura et al., 2013), performed using the gills of O. niloticus were studied. Neighbor-Joining method (Saitou and Nei, 1987) and inferred from 1000 replicates of the datasets using the bootstrap test (Felsenstein, 1985). Evolutionary distances were calculated using Material and methods the Maximum Composite Likelihood method (Tamura et al., 2004). Multiple alignments of sequences were done using Clustal Culture, isolation and characterization Omega (http://www.ebi.ac.uk/Tools/msa/clustalo). Thirty naturally infected O. niloticus were sampled and taken from El-Serw fish farm located on El Manzala Lake, Egypt. Infected Antibiotic susceptibility tests fish were characterized by typical hemorrhagic septicemia on the skin and internal organs. Live fish were transferred directly to Sensitivity analysis was carried out to 12 antibiotics by the dif- the experimental laboratory of fish diseases in the same farm to fusion method in Mueller Hinton Agar (Oxoid) and incubated at 37 detect the pathogenic bacteria. Swabs from inside each liver, kid- °C for 48 h. The tested antibiotics (Oxoid) were showed in Table 3. ney, skin and gills under aseptic precautions were inoculated into Incubation zone diameters were measured after 48 h of incubation trypticase soy broth (TSB; Oxoid) at 32 ± 1 °C for 24 h. A loopful of and classified as sensitive or resistant according to the size of the the obtained broth culture was streaked onto MacConky agar zone of the bacteria growth inhibition (CLSI, 2010). (Oxoid) and incubated at 32 ± 1 °C for 24–48 h. Morphologically similar and dominant bacterial colonies were selected and Pathogenicity assay streaked onto nutrient agar (NA) plates for 24 h at 32 ± 1 °Cin order to obtain pure isolates. After purification, isolates were re- Isolates of C. freundii,C. braakii, S. marcescens and Serratia sp. cultured on NA slants and stored at 4 °C for further identification. (OS-1, OS-2, OS-3 and OS-4, respectively) were inoculated in TSB All the bacterial isolates were characterized morphologically by and incubated at 32 ± 1 °C for 24 h. A number of 60 apparently applying Gram staining and by testing the motility of each isolate. healthy O. niloticus 80 ± 2 g was used in experiments.
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