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Isolation and Molecular Identification of the Etiological Agents of Streptococcosis in Nile Tilapia

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Isolation and Molecular Identification of the Etiological Agents of Streptococcosis in Nile Tilapia View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Hasanuddin University Repository Anshary et al. SpringerPlus 2014, 3:627 http://www.springerplus.com/content/3/1/627 a SpringerOpen Journal RESEARCH Open Access Isolation and molecular identification of the etiological agents of streptococcosis in Nile tilapia (Oreochromis niloticus) cultured in net cages in Lake Sentani, Papua, Indonesia Hilal Anshary1*, Rio A Kurniawan2, Sriwulan Sriwulan1, Ramli Ramli2 and Dolores V Baxa3 Abstract Infections with Streptococcus spp. were observed in Nile tilapia cultured in net cages in Lake Sentani, Papua, Indonesia. Clinical signs included exophthalmia, erratic swimming, ascites in abdominal cavity, and external hemorrhages. Four types of bacterial colonies (SK, K10, P20, and M12) were isolated from the brain, kidney, and eyes. Based on phenotypic and genetic (16S rDNA sequencing) characteristics, the isolates were identified as Streptococcus iniae (SK), Streptococcus agalactiae (K10 and P20) and Lactococcus garvieae (M12). The latter species has not been previously isolated or reported from fish streptococcosis in Indonesia. Intraperitoneal injection of healthy tilapia with the bacterial species caused significant morbidity (70%) within 3 days and 100% mortality at 6 days post injection. Experimental infections and reisolation of the bacteria from morbid and dead fish suggest they are the causative agents of streptococcosis, which rendered high mortality among cage cultured Nile tilapia in Lake Sentani. Our results suggest the need for developing diagnostic tools for accurate identification of the agents of streptococcosis. As tilapia aquaculture continues to expand as a means of food production and livelihood in Indonesia, it becomes crucial to ensure that fish resources are monitored and protected from the adverse effects of infectious diseases. Keywords: Streptococcosis; Nile tilapia; Cage; Lake Sentani; Streptococcus; Lactococcus garvieae Background 2012 (Working Group of Marine and Fisheries Data Nile tilapia (Oreochromis niloticus) has been the focus of Arrangement 2013), providing an important source of major aquaculture efforts worldwide because the fish is livelihood among communities along the shores of Lake easy to cultivate, adapts to a wide range of environmental Sentani, Papua, east Indonesia. Although commercial til- conditions, grows fast, tolerant to high stocking density, apia culture has been a profitable source of income for and is relatively resistant to stress and diseases (El-Sayed local fish farmers, infectious diseases have been emerging. 2006). Nile tilapia is extensively cultivated in Indonesia Streptococcosis, a bacterial disease, is one of the most particularly in Java, Sumatra, Kalimantan and Sulawesi significant diseases of tilapia worldwide. The causative Islands using various types of culture systems such as agents of the disease have been attributed to multiple pond and net cage cultures in lakes or in dams (Working bacterial agents but most commonly Streptococcus and/ Group of Marine and Fisheries Data Arrangement 2013). or Lactococcus (Kang et al. 2004; Plumb and Hanson Aquaculture of Nile tilapia in Indonesia has increased 2011). Streptococcosis is a common disease affecting considerably from 291,030 MT in 2008 to 695,063 MT in various species of fish worldwide (Roberts 2012) includ- ing the Asian seabass (Suanyuk et al. 2010), barramundi (Bromage et al. 1999), grouper (Bowater et al. 2012), * Correspondence: [email protected] Japanese flounder (Nguyen et al. 2002), rabbit fish (Yuasa 1Laboratory of Fish Parasites and Diseases, Department of Fisheries, Faculty et al. 1999), rainbow trout (Eldar and Ghittino 1999), red of Marine Science and Fisheries, Hasanuddin University, Makassar, Indonesia drum (Eldar et al. 1999; Shen et al. 2005), red tilapia Full list of author information is available at the end of the article © 2014 Anshary et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Anshary et al. SpringerPlus 2014, 3:627 Page 2 of 11 http://www.springerplus.com/content/3/1/627 (Hernandez et al. 2009; Musa et al. 2009), seabream (Evans Results et al. 2002), silver pomfret (Duremdez et al. 2004), and Bacterial isolation and biochemical characterization wild mullet (Evans et al. 2002). An annual global loss of Moribund tilapia (n = 25) were observed at 1–4 months about 250 million USD has been attributed to streptococ- following stocking in cages. Three types of Gram posi- cosis (Amal and Zamri-Saad 2011). The clinical signs of tive bacteria were isolated from the kidney (SK), brain streptococcosis or lactococcosis include unilateral or bilat- (K10 and P20), and eyes (M12). Type strains were evalu- eral exophthalmia, erratic swimming, pale gills, opaque ated for biochemical characteristics and compared to S. cornea, external haemorrhages, enlarged spleen, ascites in iniae, S. agalactiae, and L. garvieae (Table 1). All isolates abdominal cavities, and discolored liver (Suanyuk et al. were cocci in chains, non-motile, catalase negative, 2005; Salati 2011). oxidase negative, fermentative, and did not grow on Several species of Streptococcus and Lactococcus have MacConkey agar. The SK isolate was β-haemolytic while been identified as the cause of streptococcosis/lactococ- the rest were α-haemolytic. Differences in biochemical cosis in fish including Streptococcus iniae, S. agalactiae tests among the three bacterial species were observed in (synonym S. difficile), S. dysgalactiae, S. parauberis, and esculin, salicin, trehalose, and Voges Proskauer tests. S. Lactococcus garvieae (Eldar et al. 1994; Kang et al. 2004; iniae and L. garvieae fermented esculin, lactose, salicin Nomoto et al. 2004; Vendrell et al. 2006; Agnew and and trehalose, whereas S. agalactiae did not ferment the Barnes 2007; Soltani et al. 2008; Plumb and Hanson carbohydrates. L. garvieae was positive for lactose fer- 2011; Abdelsalam et al. 2013). S. iniae and S. agalactiae mentation. S. iniae, in contrast to S. agalactiae and L. have been frequently reported as the causative agents of garvieae, showed a negative VP reaction. Except for streptococcosis in tilapia worldwide (Perera et al. 1994; mannitol utilization, K10 and P20 revealed similar bio- Eldar et al. 1995; Bowser et al. 1998; Salvador et al. 2005; chemical characteristics with S. agalactiae described by Suanyuk et al. 2005, 2010; Yuasa et al. 2008; Hernandez Austin and Austin (2012). The SK isolate is similar to S. et al. 2009; Musa et al. 2009; Abuseliana et al. 2010; iniae in all biochemical characteristics. The M12 isolate Lusiastuti et al. 2012; Najiah et al. 2012; Figueiredo et al. was similar to L. garvieae except it utilized lactose but 2012). Except for one report from Brazil (Evans et al. not sorbitol (Table 1). 2009), L. garvieae has been rarely isolated in tilapia with streptococcosis. Enterococcus seriolicida, the synonym of Pathogenicity of isolates L. garvieae (Eldar et al. 1996), is the most common The four isolates that were phenotypically similar to S. causative agent of fish streptococcosis in Japan (Kusuda iniae (SK), S. agalactiae (K10 and P20), and L. garvieae et al. 1991). (M12) showed high pathogenicity to tilapia. Kaplan- In Indonesia, S. agalactiae and S. iniae have been im- Meier survival analysis showed that the mean survival plicated in streptococcosis infections in commercial cul- time of tilapia injected with S. iniae, S. agalactiae and L. ture of tilapia (Yuasa et al. 2008; Lusiastuti et al. 2012). garvieae (0.1 ml of 1.0 × 107 CFU/mL) was 2.5, 1.83, and During a monitoring survey of the health status of tilapia 3 days, respectively (Figure 1). All of the fish injected with in Lake Sentani from 2010 to 2013, severe morbidity each suspension of the bacterial isolate showed clinical and mortality were observed. Clinical symptoms in- signs and died within 6 days after injection. Morbidity or cluded long white fecal string, erratic swimming, pale mortality was not observed in the control group while the gills, opaque cornea, and exophthalmus. The isolated bacteria were recovered from morbid and dead fish in the bacteria were β-haemolytic, Gram positive, non-motile exposed injected groups. cocci, and presumptively identified as Streptococcus sp. Biochemical testing failed to identify the bacteria to the Identification of the isolates by molecular methods species level. Despite the significant losses of tilapia due The DNA of each isolate was analyzed by PCR using the to streptococcal infection in Indonesia, few studies are 16S rRNA universal primers that amplified fragments of available on the etiology of streptococcosis/lactococcosis approximately 1,500 bp in size. PCR reactions using in naturally infected fish. Furthermore, a more definitive these primers amplified a 1,482 bp from the SK isolate. identification of the causative agents using molecular Sequence alignments with known sequences in the techniques are currently lacking in Indonesia. For these GenBank database showed that the SK isolate had high reasons, the main goal of our study is to identify the similarity (99.8 − 99.9%) to S. iniae from red drum in causative agent(s) of streptococcosis among cage cul- China, Nile tilapia in Thailand, S. iniae strain ATCC tured tilapia in Lake Sentani, Papua,
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