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Comparison of Lipopolysaccharide and Protein Profiles Between Journal of Fish Diseases 2006, 29, 657–663 Comparison of lipopolysaccharide and protein profiles between Flavobacterium columnare strains from different genomovars Y Zhang1, C R Arias1, C A Shoemaker2 and P H Klesius2 1 Department of Fisheries and Allied Aquacultures, Auburn University, Auburn, AL, USA 2 Aquatic Animal Health Research Laboratory, USDA, Agricultural Research Service, Auburn, AL, USA Abstract Introduction Lipopolysaccharide (LPS) and total protein profiles Flavobacterium columnare is the causal agent of from four Flavobacterium columnare isolates were columnaris disease, one of the most important compar. These strains belonged to genetically dif- bacterial diseases of freshwater fish. This bacterium ferent groups and/or presented distinct virulence is distributed world wide in aquatic environments, properties. Flavobacterium columnare isolates ALG- affecting wild and cultured fish as well as orna- 00-530 and ARS-1 are highly virulent strains that mental fish (Austin & Austin 1999). Flavobacter- belong to different genomovars while F. columnare ium columnare is considered the second most FC-RR is an attenuated mutant used as a live vac- important bacterial pathogen in commercial cul- cine against F. columnare. Strain ALG-03-063 is tured channel catfish, Ictalurus punctatus (Rafin- included in the same genomovar group as FC-RR esque), in the southeastern USA, second only to and presents a similar genomic fingerprint. Elec- Edwardsiella ictaluri (Wagner, Wise, Khoo & trophoresis of LPS showed qualitative differences Terhune 2002). Direct losses due to F. columnare among the four strains. Further analysis of LPS by are estimated in excess of millions of dollars per immunoblotting revealed that the avirulent mutant year. Mortality rates of catfish populations in lacks the higher molecular bands in the LPS. Total ponds can reach 50–60% and can be as high as protein analysis displayed by immunoblotting 90% in tank-held catfish fingerlings (USDA showed differences between the strains analysed 2003a,b). although common bands were present in all the Columnaris disease usually begins as an external isolates. FC-RR lacked two distinct common bands infection of fins, body surface or gills. The fins (34 and 33 kDa) shared by the other three isolates. become necrotic with greyish to white margins, Based on the difference of LPS and total protein and initial skin lesions appear as discrete bluish profiles, it is possible to discriminate the attenuated areas that evolve into depigmented necrotic mutant FC-RR from other F. columnare strains. lesions. Skin lesions may have yellowish mucoid material accompanied by mild inflammation. Keywords: Flavobacterium columnare, genomovars, Lesions can develop exclusively on the gills, which lipopolysaccharide, modified live vaccine, virulence, usually results in subacute disease and mortality, whole protein profiles. as is typically the case in young fish (Plumb 1999). Due to the ubiquitous presence of F. columnare in aquatic environments, eradication of the disease in fish farms is not likely to occur. Control and treatment of columnaris have primarily been direc- Correspondence C R Arias, 203 Swingle Hall, Auburn University, Auburn, AL 36849, USA ted towards the use of improved water-management (e-mail: [email protected]) practices to reduce physiological and environmental Ó 2006 Blackwell Publishing Ltd 657 Journal of Fish Diseases 2006, 29, 657–663 Y Zhang et al. LPS and total protein comparison in F. columnare stress in the fish. Recently, a modified live F. col- from diseased channel catfish at the Alabama Fish umnare vaccine has been developed using a rif- Farming Center, Greensboro, AL. The ARS-1 ampicin-resistant strategy (Shoemaker, Klesius & isolate was recovered from diseased channel catfish Evans 2005b). This methodology was previously at the Aquatic Animal Health Research Unit, used by Montaraz & Winter (1986) to generate a USDA-ARS, Auburn, AL. These two isolates have rough Brucella abortus strain, currently employed as been demonstrated to be virulent for channel catfish the official vaccine for cattle brucellosis in the USA. (Shoemaker, Klesius, Lim & Yildirim 2003a; The same strategy was used by Klesius & Shoe- Welker, Shoemaker, Arias & Klesius 2005). maker (1999) to create an Edwardsiella ictaluri Flavobacterium columnare ALG-03-063 was also rifampicin-resistant mutant patented as a modified included because it was isolated from diseased live vaccine against enteric septicaemia of catfish channel catfish and was the genetically most similar (ESC) (AQUAVAC-ESCÒ; Intervet, Millsboro, strain to the avirulent mutant FC-RR present in our DE, USA). Characterization of B. abortus and collection. E. ictaluri rifampicin-resistant mutants revealed that lipopolysaccharide (LPS), a main virulence Genetic fingerprinting factor for Gram-negative bacteria, lacked the high molecular bands observed in virulent isolates (Kle- A previous study by Arias, Welker, Shoemaker, sius & Shoemaker 1999; Vemulapalli, McQuiston, Abernathy & Klesius (2004) divided F. columnare Schurig, Sriranganathan, Halling & Boyle 1999; strains into four well-defined genetic groups. All Arias, Shoemaker, Evans & Klesius 2003). catfish isolates were grouped into three different Flavobacterium columnare belongs to the Cyto- genogroups (I–III; genogroup IV included only phaga–Flavobacterium–Bacteroid group and is tilapia isolates). Strains ALG-00-530 and ARS-1 phylogenetically distant from the better studied belong to genogroups I and II, respectively; subclass Gammaproteobacteria, which contains while ALG-03-063 belongs to genogroup III. major human and animal pathogens (including The avirulent mutant FC-RR was not included Brucella and Edwardsiella). To date, virulence factors in that study but was fingerprinted in the present in F. columnare are poorly characterized. Specifically, work. Amplified fragment length polymorphism the role of LPS in columnaris pathogenicity has not (AFLP) patterns from the FC-RR mutant were been explored. The main objective of this study was obtained as described by Arias et al. (2004), added to investigate whether an attenuated F. columnare to the existing database and analysed. mutant originated through a rifampicin-resistance strategy presented a modified LPS and a different Production of polyclonal antiserum against total protein profile by comparison with virulent Flavobacterium columnare strains. Twelve channel catfish were randomly divided into three groups of four fish each. Two groups Materials and methods were used to produce antibodies (Ab) against the ALG-00-530 and FC-RR F. columnare strains Bacterial isolates and culturing (Ab-ALG-00-530 and Ab-FC-RR) while the third Four F. columnare strains, ALG-00-530, FC-RR, group served as a negative control. Antigen ARS-1 and ALG-03-063 were used in this study. preparation was performed according to Arias The FC-RR strain is a rifampicin-resistant mutant, et al. (2003) with the following modifications: avirulent for catfish (Shoemaker et al. 2005b). This cells were grown overnight in modified Shieh attenuated mutant has been licensed as a modified broth and control fish were also inoculated with live vaccine by Intervet, Inc. and it is now Shieh broth. Three weeks after booster immuniza- undergoing field trials (Patent no.: US tion, fish were bled and antiserum was used to 6 881 412B1). Unfortunately, the original parent probe Western blots (see below). In order to strain used to derive the avirulent mutant could not determine the relative titre of the sera, enzyme- be included in this work as it lost viability during linked immunosorbent assays (ELISA) were con- storage. Instead, other comparable (same geograph- ducted according to Shoemaker, Shelby & Klesius ical origin and source) virulent F. columnare strains (2003b). Serum from each individual fish was were analysed. Isolate ALG-00-530 was obtained tested against each antigen dilution. Ó 2006 Blackwell Publishing Ltd 658 Journal of Fish Diseases 2006, 29, 657–663 Y Zhang et al. LPS and total protein comparison in F. columnare After blotting, one membrane was incubated with Lipopolysaccharides and total protein extraction anti-ALG-00-530 serum while the second mem- The four isolates were cultured in modified Shieh brane was incubated with anti-FC-RR serum. After broth for 24 h at 28 °C. Three millilitres of broth blocking for 30 min, 1:500 diluted polyclonal was centrifuged at 3000 g for 15 min. Pelleted cells catfish serum was incubated with the membrane were resuspended in lysis buffer and proteins were overnight followed by 1-h incubations with a extracted according to Arias, Verdonck, Swings, monoclonal antibody (E-8) specific for channel Aznar & Garay (1997a). Crude LPS was extracted catfish IgM (1:10) (Klesius 1990), and labelled with following the phenol–water protocol described by conjugated goat antimouse Ig (1:5000), followed by Westphal & Jann (1965). After lyophilization, the detection with Opti-4CNTM (Bio-Rad). LPS extract was diluted in sample buffer at a final ) concentration of 1 mg mL 1. Aqueous and phenol LPS phases were stored at )80 °C until use. Results Amplified fragment length polymorphism analysis Lipopolysaccharides and total protein analysis Figure 1 shows the results of the cluster analysis of Electrophoresis the AFLP patterns from the strains used in this Lipopolysaccharides from both phases were resus- study. Attenuated mutant FC-RR displayed a pended in sample treatment buffer and electro- unique AFLP fingerprint although it clustered phoresed by discontinuous sodium dodecyl among other
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