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1 Laboratorium voor Microbiologie, Ghent University, K.L. Ledeganckstr. 35, B-9000 Ghent, Belgium
2 Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK
3 Institut für Angewandte Mikrobiologie, Justus-Liebig-Universität Giessen, IFZ, Heinrich-Buff-Ring 26–32, D-35392 Giessen, Germany
4 Laboratorium voor BCCMTM/LMG Bacteria Collection, Ghent University, K.L. Ledeganckstr. 35, B-9000 Ghent, Belgium
Correspondence
Geert Huys
geert.huys{at}rug.ac.be
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ABSTRACT |
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99·0 % 16S rDNA sequence similarity with the type strains of the two A. hydrophila subspecies. DNA–DNA hybridization with type and reference strains of all known Aeromonas taxa revealed that the Au group represented a homogeneous taxon that exhibited the highest relatedness with members of the two A. hydrophila subspecies, ranging from 75 to 93 %. Phenotypic characterization on the basis of 152 features further revealed that the Au group isolates differed from A. hydrophila subsp. hydrophila or subsp. dhakensis in a total of 13 biochemical properties. Of these, assimilation of L-glycine and isobutyrate as sole carbon source, acid production from salicin and D-sucrose, and aesculin hydrolysis were of diagnostic value. From the results of this study, it can be concluded that the Aeromonas frog isolates of the Au group represent a new subspecies of A. hydrophila, for which the name Aeromonas hydrophila subsp. ranae subsp. nov. is proposed. Its type strain is Au-1D12T (=LMG 19707T=CCUG 46211T).
Published online ahead of print on 29 November 2002 as DOI 10.1099/ijs.0.02357-0.
The EMBL accession number for the 16S rDNA sequence of Au strain LMG 19707T is AJ508766.
Supplementary tables are available in IJSEM Online.
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) and as opportunistic human pathogens (Janda & Abbott, 1996). Historically, the pathogenicity of aeromonads was first established with poikilotherms. In Southeast Asia, outbreaks of motile Aeromonas-associated septicaemia can reach epidemic proportions among farmed aquatic animals, leading to massive mortality rates (Joseph & Carnahan, 1994). Strains of Aeromonas hydrophila are also pathogenic for amphibians, including turtles (Pasquale et al., 1994) and frogs. Occasionally, motile aeromonad septicaemia in frogs has also been cited as ‘red leg’ disease, referring to haemorrhages that were occasionally observed in the leg muscles of diseased animals (Rigney et al., 1978). However, identification data are only rarely reported in studies on bacterial septicaemic disease of frogs and are often based on primary phenotypic characterization. During a survey of frogs farmed in Thailand, including the species Rana rugulosa (Chinese bullfrog) and Rana tigerina (Indian bullfrog or tiger frog), Pearson et al. (1997) isolated a collection of motile aeromonads from the skin and intestine of both healthy and septicaemic adult frogs. Next to representatives of A. hydrophila, Aeromonas veronii and Aeromonas caviae, a group of unspeciated strains designated group Au was recovered exclusively from the internal organs of septicaemic animals surveyed at different farms throughout Thailand. The Au group was found to be biochemically distinct from the former species because all strains failed to ferment or assimilate D-sucrose, a characteristic which is also common to the species Aeromonas eucrenophila (Huys et al., 1997a), Aeromonas schubertii (Hickman-Brenner et al., 1988), Aeromonas jandaei (Carnahan et al., 1991) and Aeromonas popoffii (Huys et al., 1997b). In addition, randomly amplified polymorphic DNA (RAPD) analysis revealed a genotypic homogeneity that was unusual for a group of geographically diverse Aeromonas isolates (Pearson et al., 1997). The current investigation was initiated to determine the taxonomic position of the unknown Au group in the genus Aeromonas by subjecting a group of seven representative strains to fluorescent amplified fragment length polymorphism (FAFLP) and ERIC-PCR fingerprinting, 16S rDNA sequencing, extensive phenotypic characterization and microplate DNA–DNA hybridization. The data generated indicate that the Au group genotypically belongs to A. hydrophila DNA hybridization group (HG) 1 but constitutes a phenotypically unique taxon in this species, for which the name A. hydrophila subsp. ranae is proposed.
Seven Aeromonas isolates belonging to the Au group (LMG 19707T–LMG 19713) recovered from the liver or kidney of septicaemic Rana rugulosa at various farm sites in Thailand were included in the present study (additional descriptive data are available as supplementary Table 1 in IJSEM Online at http://ijs.sgmjournals.org). Type and reference strains of all known Aeromonas species were obtained from the BCCM/LMG Bacteria Collection, Ghent University, Belgium. All strains were cultured aerobically on Trypticase soy agar (TSA) containing 3 % (w/v) Trypticase soy broth (BBL) and 1·5 % (w/v) bacteriological agar no. 1 (Oxoid) at 28 °C for 24 h. All Au isolates were subjected to (FAFLP) fingerprinting and the resulting band profiles were compared with the laboratory-based AEROLIB library (Huys & Swings, 1999). Microscale DNA extraction, AFLP template preparation, selective PCR amplification, electrophoresis on an automated DNA sequencer and data processing were performed as previously described (Huys & Swings, 1999). Microscale DNA extracts were also used for repetitive-sequence-based PCR fingerprinting using the ERIC1R and ERIC2 oligonucleotide primers (Versalovic et al., 1991). ERIC-PCR analysis was performed twice during independent runs according to the protocol of Versalovic et al. (1994) with minor modifications reported by Huys et al. (2002). All Au frog isolates were tested for 152 physiological and biochemical properties as previously described (Huys et al., 1997b). The urocanic acid assimilation test was performed according to Hänninen (1994). A total of 30 features were selected for repeated determinations. For all strains under study, both readings gave identical results, demonstrating the excellent reproducibility of the method. Antimicrobial susceptibilities were determined for six antimicrobial agents with the disc diffusion method. The following antibiotic discs (Oxoid) were applied using a ST6090 Disc Dispenser (Oxoid): nalidixic acid (30 µg), penicillin (10 µg), ampicillin (25 µg), tetracycline (30 µg), kanamycin (30 µg) and streptomycin (25 µg). Antibiograms were determined according to the conventional Kirby–Bauer method (Bauer et al., 1966) with the exception that Meuller–Hinton medium was replaced by IS broth and ISA medium (Traub et al., 1998). Isolates were classified into three categories based on the quantitative interpretation criteria recommended by the National Committee for Clinical Laboratory Standards (1993). Au strains LMG 19707T, LMG 19709 and LMG 19711 were used in a DNA–DNA hybridization study that also included the type strains of all known Aeromonas species. Genomic DNA was prepared using a combination of the protocols of Marmur (1961) and Pitcher et al. (1989) as described by Goris et al. (1998). Hybridizations were performed using the fluorometric microplate method (Ezaki et al., 1989) with modifications by Goris et al. (1998) at an optimal renaturation temperature of 45 °C. Fluorometric data recorded after 15 min incubation were used for calculation of the DNA–DNA hybridization values. The complete 16S rDNA sequences of strains LMG 19562T and LMG 19707T were determined as previously described (Huys et al., 2001) using the ABI PRISM 3100 Genetic Analyser.
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). In the current study, the digitized FAFLP banding patterns of the Au isolates were compared with the laboratory database AEROLIB comprising well-characterized strains of all known Aeromonas taxa. This comparison, of which a simplified version including only the type strains of other Aeromonas spp. is depicted in Fig. 1, revealed that the seven Au isolates represent a homogeneous cluster delineated at a correlation level of 68 %. This cluster constitutes a subgroup within the AFLP group representing A. hydrophila as witnessed by its close genotypic relatedness to members of A. hydrophila subsp. hydrophila (51 % correlation) and, to a lesser extent, of A. hydrophila subsp. dhakensis (33 % correlation). The latter two taxa were recently described by Huys et al. (2002) to allocate two groups of A. hydrophila HG1 strains that were sufficiently different on a phenotypic basis to warrant their definition as separate subspecies. Visual comparison of ERIC-PCR fingerprints allowed a group of six Au isolates to be distinguished from a collection of nine reference strains encompassing the two A. hydrophila subspecies (Fig. 2). This differentiation was based on visual scoring of the band with an estimated size of 0·7 kb that is present in the ERIC-PCR profiles of all Au strains but absent in members of the two A. hydrophila subspecies. In addition, the lack of an ERIC-PCR fragment approximately 0·95 kb in size allowed the further differentiation of the Au isolates from A. hydrophila subsp. hydrophila strains that all exhibited this band in their profiles. Although the stability of these group-specific ERIC-PCR markers was demonstrated by performing duplicate experiments, it is clear that their taxonomic value should be further monitored by other workers eventually including additional Au-group-like isolates. Taken together, the AFLP and ERIC-PCR data suggest that the Au isolates are closely affiliated to A. hydrophila HG1 although they seem to constitute a separate genotypic subgroup in this taxon.
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in IJSEM Online at http://ijs.sgmjournals.org) clearly confirm the genotypic position of the Au group as exhibited by numerical analysis of FAFLP profiles (Fig. 1
). The internal genomic relatedness of the Au group as determined from strains LMG 19707T, LMG 19709 and LMG 19711 ranged from 93 to 103 %, indicating that the Au strains constitute a genotypically homogeneous group in the genus Aeromonas. In concordance with FAFLP clustering, a high relatedness was also found between the three representatives of the Au group and the type strain and two reference strains of A. hydrophila subsp. hydrophila (80–93 %), and with the type strain of A. hydrophila subsp. dhakensis (75–87 %). On the basis of DNA–DNA hybridization values ranging from 46 to 64 %, Au strains LMG 19707T and LMG 19711 could be clearly distinguished from the type strains of other Aeromonas spp. Collectively, the results from the DNA–DNA hybridization experiments clearly indicate that the Au group should be located in the species A. hydrophila.
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), these results indicate that the isolates of the Au group are phylogenetically closely affiliated to the species A. hydrophila HG1.
The absence of sucrose assimilation and fermentation, as displayed by all Au strains, is considered highly atypical within A. hydrophila HG1 (Huys et al., 2002). In fact, the Au group was characterized overall by a relatively narrow spectrum of carbon sources that could be utilized or fermented. In addition to the urocanic acid test, a total of 12 negative test results allowed the differentiation of the group of Au isolates from A. hydrophila subsp. hydrophila and/or subsp. dhakensis because of this uniform biochemical inertness (Table 1). Among these tests, assimilation of L-glycine and isobutyrate as sole carbon source, acid production from salicin and D-sucrose, and aesculin hydrolysis were essential for the unequivocal separation of the Au group from both A. hydrophila HG1 subspecies. Collectively, the finding of at least 13 discriminative features (Table 1) indicates that the Au group does not belong to A. hydrophila subsp. hydrophila or subsp. dhakensis and thus represents a third phenotypic subgroup in this species. All Au isolates were lysine decarboxylase- and arginine dihydrolase-positive, utilized DL-lactate, and failed to form acid from sorbitol and L-rhamnose. These characteristics are also shared by the two subspecies currently situated in A. hydrophila (Table 2; Huys et al., 2002) and can thus be considered species-specific. As a member of the species A. hydrophila, the Au group can be phenotypically differentiated from Aeromonas salmonicida by its motility, its ability to grow at 37 °C and/or its inability to produce a brown water-soluble pigment (Pavan et al., 2000). Furthermore, at least two tests are available for the separation of the Au group from each of the other species that are currently recognized in the genus Aeromonas (Table 2).
The DNA–DNA hybridization results and the 16S rDNA sequencing and phenotypic data reported in this study indicate that the Au group represents a new phenotypic subtaxon in the species A. hydrophila which deserves subspecies status in addition to the currently delineated subsp. hydrophila and subsp. dhakensis (Huys et al., 2002). We propose the name Aeromonas hydrophila subsp. ranae for the seven Au strains.
Description of Aeromonas hydrophila subsp. ranae subsp. nov.
Aeromonas hydrophila subsp. ranae (ra'.nae. N.L. fem. n. Rana generic name of frog; N.L. gen. n. ranae, of a frog).
All strains of the newly proposed subspecies were isolated from farmed frogs in Thailand. All strains of Aeromonas hydrophila subsp. ranae display the following characteristics typical of the genus Aeromonas: Gram-negative straight motile rods, chemo-organotrophic with both oxidative and fermentative metabolism, and cytochrome oxidase and catalase are positive. Optimal growth occurs after 24 h at 28 °C on TSA medium. No brown water-soluble pigment is produced on TSA medium. Arginine dihydrolase, lysine decarboxylase and indole are positive. Three out of the seven strains, i.e. LMG 19709, LMG 19710 and LMG 19713, are Voges–Proskauer-positive. Urease, tryptophan deaminase, ornithine decarboxylase and H2S are not produced. The following substrates are used as the sole carbon and energy sources: L-alanine (except strains LMG 19710 and LMG 19712), arbutin, L-arginine, L-aspartate (except strains LMG 19710 and LMG 19713), D-fructose, fumarate, D-galactose, D-gluconate, D-glucosamine, D-glucose, glycerol, L-histidine, DL-lactate, L-malate, D-mannitol, D-mannose, D-maltose, L-proline, pyruvate, D-ribose, L-serine, succinate and D-trehalose. None of the strains use acetamidocaprate, N-acetyl-D-galactosamine, cis-aconitate, trans-aconitate, adipate, adonitol, 4-aminobutyrate, L-arabinose, D-arabitol, DL-aspartate (except strain LMG 19707T), azelate, betaine, cadaverine, caprate, D-cellobiose, L-citrulline, erythritol, D-fucose, L-fucose, D-glucosaminic acid, D-glucuronate, glutarate, D-glutamate, L-glycine, 3-hydroxybenzoate, 4-hydroxybenzoate, inositol, isobutyrate, isovalerate, itaconate, lactose, lactulose, L-leucine, L-lysine, maltitol, D-melibiose, mesaconate, 
-methyl D-mannoside, L-ornithine (except strain LMG 19707T), phenylacetate, L-phenylalanine, propionate, D-raffinose, L-rhamnose, sorbate, D-sorbitol, spermidine, spermine, suberate, D-sucrose, L-tryptophan, L-valine, D-xylitol or D-xylose. Acid is uniformly produced from D-glucose, D-maltose, D-mannitol, D-mannose and D-trehalose, but not from adonitol, amygdalin, L-arabinose, D-arabitol, D-cellobiose, dulcitol (except strain LMG 19711), erythritol, inositol, -D-melibiose, methyl-D-glucoside, lactose, D-raffinose, L-rhamnose, salicin, D-sorbitol, D-sucrose or D-xylose. All strains hydrolyse the following substrates: L-alanine-pNA, 2-deoxythymidine-5'-pNP-phosphate, gelatin, bis-pNP-phosphate, ortho-nitrophenyl-
-D-galactopyranoside, pNP--D-glucopyranoside, pNP-phenylphosphonate, pNP-phosphoryl choline and L-proline-pNA. None of the strains are able to hydrolyse aesculin, L-glutamate-
-3-carboxy-pNA, pNP--D-glucopyranoside or pNP--D-glucuronide. All strains are resistant to ampicillin and penicillin but sensitive to kanamycin (except strain LMG 19711), streptomycin (except strain LMG 19711) and tetracycline. Strains LMG 19707T, LMG 19709, LMG 19710 and LMG 19713 were resistant to nalidixic acid. Isolated in 1994 from the liver and kidneys of septicaemic farmed frogs (Rana rugulosa) in Thailand.
The type strain has been deposited in the BCCM/LMG Bacteria Collection, Ghent University (Belgium), as strain LMG 19707T and in the CCUG Culture Collection, University of Göteborg (Sweden), as strain CCUG 46211T.
Significance of Aeromonas hydrophila subsp. ranae as a poikilotherm pathogen
Recently, Pearson et al. (2000) reported on the virulence properties of 11 Aeromonas isolates belonging to the Au group. All these isolates displayed high haemolytic activities conferred by ASH1, a haemolysin gene previously cloned from an A. salmonicida strain (Hirono & Aoki, 1993) that was not found in other non-Au frog Aeromonas isolates. Furthermore, most Au strains produced elastase and were highly cytotoxic to rainbow trout cells but did not significantly affect a mammalian cell line (Pearson et al., 2000). In a supplementary study, clinically healthy Rana rugulosa that were challenged with isolates of the Au group reproduced the symptoms of Aeromonas-associated septicaemia, resulting in mortalities (M. Pearson, unpublished data). During these challenge trials, Koch's postulates were fulfilled and thus confirmed that strains of the Au group are the causal agents of septicaemia in farmed frogs. Further studies should elaborate on the role of the ASH1 gene product in the pathogenesis of motile Aeromonas septicaemias of farmed frogs and other aquatic species.
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ACKNOWLEDGEMENTS |
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