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1 Departamento de Microbiología y Ecología, Facultad de Biología, Universitat de València, E-46100 Burjassot (Valencia), Spain
2 Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Sevilla, E-41012 Sevilla, Spain
Correspondence
Consuelo Esteve
estevem{at}uv.es
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Published online ahead of print on 7 March 2003 as DOI 10.1099/ijs.0.02504-0.
Details of the strains used in this study, LD50 values of A. jandaei-like strains and a dendrogram based on the SSM/UPGMA analysis are available as supplementary material in IJSEM Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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, 1988; Schubert et al., 1990a, b; Carnahan et al., 1991a, b; Martínez-Murcía et al., 1992b). These two species show 99·5 % similarity in their complete 1502 bp 16S rDNA sequences (Martínez-Murcía et al., 1992a), but they can clearly be segregated by DNA–DNA hybridization methods (Carnahan et al., 1991a). In fact, the species A. veronii and A. jandaei are synonyms of DNA homology groups (DHG) 8/10 and 9, respectively, of the genus Aeromonas (Joseph & Carnahan, 2000).
The present taxonomic status of A. veronii is based mainly on genomic data (Hickman-Brenner et al., 1987; Martínez-Murcía et al., 1992a), since its biogroups veronii and sobria are not phenotypically related (Kämpfer & Altwegg, 1992; Valera & Esteve, 2002). In fact, A. veronii biogroup sobria displays closer phenotypic resemblance to A. jandaei, as phenotypic differentiation between these taxa is based only on acid production from sucrose, which is positive for A. veronii biogroup sobria but negative for A. jandaei (Carnahan et al., 1991c; Abbot et al., 1992). On the other hand, the limits of A. veronii biogroup sobria have recently been extended by the inclusion of the type strain of Aeromonas ichthiosmia (Huys et al., 2001).
Although A. jandaei was formerly associated with clinical samples, the reported incidence of this taxon in human disease is extremely low (Janda et al., 1994; Bravo et al., 1995; Hänninen et al., 1995; Kühn et al., 1997; Borrell et al., 1998; Ghenghesh et al., 1999; Demarta et al., 2000). By contrast, presumptive A. jandaei strains have frequently been isolated from cultured eels suffering from ‘red fin disease’ (Esteve et al., 1993; Valera & Esteve, 2002). However, these environmental strains were somewhat related to A. veronii biogroup sobria, as they produced acid from sucrose. The aim of the present study was to determine the taxonomic position of these novel isolates in relation to reference strains representative of recognized Aeromonas species (A. jandaei, A. veronii, Aeromonas sobria, A ichthiosmia, Aeromonas enteropelogenes, Aeromonas trota, Aeromonas allosaccharophila and Aeromonas popoffii).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). These strains, which were mainly associated with epizootic outbreaks that occurred in eel farms from 1987 to 1998, were stored long-term as freeze-dried cultures. The 43 reference strains used in the study are detailed in Supplementary Table B (available in IJSEM Online). Strains were grown overnight on tryptone water [1 % (w/v) tryptone, 0·5 % (w/v) NaCl in distilled water; pH 7·2] or tryptone soy agar (Oxoid) at 28 °C.
Phenotypic characterization and numerical taxonomy.
Each strain (57 strains and six duplicate cultures) was examined for 121 physiological and biochemical traits, as described previously (Valera & Esteve, 2002). Production of 
-haemolysins against human erythrocytes was tested on solid medium according to Esteve (1995). The tests results were scored as 1 for positive responses and 0 for negative responses; these data were examined with the NTSYS-pc numerical taxonomy and multivariance analysis system (Rolhf, 1998). Similarities were calculated using both simple matching (SSM) and Jaccard (SJ) coefficients; clustering was achieved by the UPGMA method and cophenetic correlation was calculated using the correlation coefficient r (Sneath & Sokal, 1973). Test error was calculated according to Sneath & Johnson (1972).
DNA base composition.
Previously described procedures (Marmur, 1961; Johnson, 1994) were used to extract and purify DNAs from 29 Aeromonas strains (Table 1). The DNA G+C content of the strains was obtained from the midpoints (Tm) of the thermal denaturation profiles (Marmur & Doty, 1962; Ferragut & Leclerc, 1976; Owen & Hill, 1979). The Tm of DNA from Escherichia coli NCTC 9001T was determined experimentally and was used as a reference.
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). DNAs from reference strains (CECT 4228T, CECT 4486T, CECT 4257T and CECT 4835) were denatured and then bound to a nitrocellulose filter or labelled with [3H]dCTP (Amersham). Each hybridization mixture included the following: (i) filter containing unlabelled reference single-stranded (ss) DNA, (ii) labelled homologous ssDNA, (iii) unlabelled competitor ssDNA and (iv) 30 % formamide (Sigma). The ratio of the concentrations of labelled homologous ssDNA and unlabelled competitor ssDNA was equal to or less than 1 : 150. DNA–DNA hybridizations were made at a reassociation temperature of 55·5–56·0 °C, depending on the values of DNA Tm. All hybridization experiments were performed in triplicate. In some cases, the results showed in Table 1
are values of DNA relatedness obtained from two different hybridization experiments. Percentage relatedness was calculated as described previously (Johnson, 1994). In addition, the SD was calculated for each hybridization experiment according to Sokal & Rohlf (1969).
Pathogenicity.
Animal models were used to assess potential pathogenicity of A. jandaei DHG9 strains. Juvenile European eels (5–12 g) and 6-week-old mice (19–31 g) were used in the infection trials. For each strain, six animals were anaesthetized and challenged with the same bacterial dose (108, 107, 106, 105, 104 or 103 cells). Six animals injected with sterile PBS were used as a negative control. Mortalities in a 7 day period were only considered if the injected bacterium was reisolated as a pure culture from freshly dead animals. The LD50 of bacterial cells was calculated for each strain (Reed & Müench, 1938).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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=0·0097), which is an acceptable value according to Sneath & Johnson (1972). Consistent results were obtained from the phenotypic study, as nearly the same dendrogram was derived by the use of the two similarity coefficients (SSM and SJ) and UPGMA clustering algorithm. In this study, SJ/UPGMA analysis was chosen because the correlation observed between the similarity matrix and the corresponding tree matrix (r=0·90) was higher than that presented for SSM/UPGMA analysis (r= 0·86). Seventy-seven per cent of strains were grouped by the SJ/UPGMA analysis into nine phenons defined at or above 81·6 % similarity (Fig. 1). The SSM/UPGMA analysis yielded almost identical grouping at similarity values of 
90 %, although the percentage of total clustered strains was slightly higher (81 %). A dendrogram based on the SSM/UPGMA analysis is shown in Supplementary Fig. A, available in IJSEM Online.
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) regarding the high percentages of sucrose- and elastase-positive strains observed (Table 2). In contrast to data reported previously (Hasan et al., 1992), all A. jandaei strains displayed elastolytic activity on the medium of Hsu et al. (1981). In our opinion, this medium might enhance the elastolytic capability of strains as it contains large amounts of ground elastin (1 %, w/v) but very small amounts of tryptone (0·2 %, w/v) and it also contains micronutrients (L-cysteine and Ca2+ ions) that stabilize elastase structure and function. Moreover, the pH of the medium is buffered to 8·0, which is optimal for most reported elastases (Wretlind & Wadström, 1977; Kothary & Kreger, 1985).
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). This supra-group, ‘A. jandaei–A.veronii biogroup sobria–A. ichthiosmia’, was linked at 80·7 % similarity (SJ) and was clearly segregated from the other Aeromonas species (Fig. 1). In fact, we have observed that the phenotypic core of the species A. veronii biogroup sobria corresponded to phenons 5, 6 and 7 (Fig. 1). These clusters grouped 36 % of the total A. veronii biogroup sobria strains, among them strain Popoff 224 (CECT 4835), which is a reference strain for the genospecies DHG8 (Joseph & Carnahan, 2000). Our results are in agreement with the previous numerical study by Kämpfer & Altwegg (1992), in which these reference strains of A. veronii biogroup sobria were grouped in two well-segregated clusters. Thus, diversity inside the taxon A. veronii biogroup sobria could be much higher than is currently recognized (Abbot et al., 1992; Martinetti Lucchini & Altwegg, 1992; Huys et al., 2001). In view of these overall results, for the genomic study, we used all strains that clustered in the supra-group ‘A. jandaei–A.veronii biogroup sobria–A. ichthiosmia’ (Fig. 1) as well as the reference strains of A. veronii (biogroup veronii CECT 4257T; biogroup sobria CECT 4835).
As expected, the two biogroups of A. veronii were not related phenotypically, as all reference strains of A. veronii biogroup veronii were clustered in phenon 4 (Fig. 1). Moreover, our numerical analysis clearly segregated the species A. allosaccharophila (phenon 8) from the A. veronii taxon, in contrast to other studies (Huys et al., 1996, 2001). Finally, we should note that all reference strains of the species A. trota were clustered in phenon 9, along with strain CECT 4814 (Fig. 1), which had been received as a reference strain for A. jandaei.
Genomic study: DNA base composition and DNA–DNA relatedness
The DNA G+C contents of strains included in the ‘A. jandaei cluster’ (phenon 1) ranged from 58·1 to 61·1 mol% (Table 1). This range of three units is similar to that described among bacterial strains belonging to a single Aeromonas species (Popoff et al., 1981; Hickman-Brenner et al., 1987; Esteve et al., 1995b). The DNA G+C contents of strains clustered in phenons 2 and 3 were respectively within the ranges 61·1–61·9 mol% and 60·0–60·7 mol% (Table 1). It is noteworthy that the DNA G+C contents of all these strains are being reported for the first time, even those of strains included in the original description of the species A. jandaei (Carnahan et al., 1991a). As expected, the overall values obtained for DNA G+C content (Table 1) were within the range reported for the genus Aeromonas (57·0–63 mol%) (Popoff et al., 1981; Popoff, 1984; Allen et al., 1983; Hickman-Brenner et al., 1987; Schubert & Hegazi, 1988; Schubert et al., 1990a, b; Esteve et al., 1995a, b; Huys et al., 1997).
Except for isolates E273, AO62 and M6, DNA relatedness among strains grouped in the ‘A. jandaei cluster’ (phenon 1) and the type strain, A. jandaei CECT 4228T, ranged from 70 to 100 % (Table 1), values currently accepted for the definition of a bacterial species (Stackebrandt & Goebel, 1994). In addition, reciprocal DNA–DNA hybridizations performed between some strains clustered in phenon 1 (E30, CECT 4910 and S345) and the type strain, CECT 4228T, yielded values in the range 75–87 %. Thus, these strains, which include many sucrose-positive A. jandaei-like isolates and the clinical strain CECT 4910, should be classified as members of genospecies 9 (DHG9), and they therefore belong to the A. jandaei taxon. As expected, DNA relatedness between A. jandaei DHG9 strains and representative strains of A. ichthiosmia (CECT 4486T) and A. veronii (CECT 4257T, CECT 4835) was well under 70 % (Table 1). Thus, DNA–DNA hybridizations clearly segregated A. jandaei DHG9 from the taxa A. ichthiosmia and A. veronii, although they are close relatives on the basis of 16S rDNA sequence comparison (Martínez-Murcía et al., 1992a; Collins et al., 1993) and phenotypic features (Fig. 1).
Reciprocal DNA–DNA hybridizations performed between A. ichthiosmia CECT 4486T and reference strains of A. veronii (biogroup veronii CECT 4257T; biogroup sobria CECT 4835) yielded values of around 45 % DNA relatedness (Table 1). In fact, our data agree with the value of 60 % DNA relatedness originally reported for the pair A. ichthiosmia CECT 4486T/A. veronii CECT 4835 (Schubert et al., 1990b) by using the spectrophotometric method (De Ley et al., 1970). In contrast, they contradict the value of 96 % DNA relatedness recently reported for the pair A. ichthiosmia CECT 4486T/A. veronii CECT 4257T (Huys et al., 2001) by using the micro-well hybridization method of Goris et al. (1998). It is worth noting that Huys et al. (2001) used these DNA relatedness data to propose that A. ichthiosmia is a later synonym of A. veronii. However, in our opinion, this proposal should be reconsidered on the basis of the striking lack of concordance between these hybridization studies (Huys et al., 2001; Schubert et al., 1990b; Table 1).
On the other hand, the peripheral A. veronii biogroup sobria strains (phenons 2 and 3) were related to the species A. jandaei, A. ichthiosmia and A. veronii at levels of DNA relatedness below 50 % (Table 1), and they therefore do not belong to any of these taxa. It is worth noting that DNA relatedness between strains CECT 4902, CECT 4903, CECT 4906 and CECT 4911 and A. veronii (CECT 4257T, CECT 4835) is reported here for the first time (Table 1), even though these four strains have been widely used as reference strains for A. veronii biogroup sobria DHG8 (Huys et al., 1996, 2001). However, according to our results, these four strains should not be assigned to the species A. veronii, indicating that the biogroup sobria is a heterogeneous taxon that requires further revision. In fact, strain CECT 4911 has recently been classified as A. allosaccharophila on the basis of gyrB gene sequencing data (Yáñez et al., 2003).
The genomic relationship between the reference strains of A. veronii biogroup sobria DHG8 (CECT 4835) and A. veronii biogroup veronii DHG10 (CECT 4257T) was closer (Table 1) than the current limit for species definition (70 %) and our data are therefore in agreement with previous reports that classified them in the A. veronii taxon (Hickman-Brenner et al., 1987; Martínez-Murcía et al., 1992a; Yáñez et al., 2003).
The overall SD of DNA relatedness determined in our competitive hybridization study, at around 6 %, is comparable to other studies based on the micro-well (Goris et al., 1998; Christensen et al., 2000) and spectrophotometric methods (Angen et al., 1999). Moreover, we have observed that the mean SD of high DNA similarity data (70 %) was around 2 %, this value being significantly below the 7 % recorded as the mean SD for low DNA similarity data (<70 %).
In summary, the present phenotypic and genotypic data support the classification of the A. jandaei-like strains, as well as strain CECT 4910, previously assigned to A. veronii biogroup sobria, in the species A. jandaei. Thus, we propose the emendation of the species A. jandaei to include these novel clinical and environmental isolates.
Phenotypic differentiation of the species A. jandaei
A. jandaei can be differentiated easily from the species A. veronii biogroup veronii, Aeromonas hydrophila, Aeromonas bestiarum, Aeromonas eucrenophila and Aeromonas encheleia by the absence of production of acid from salicin and its inability to hydrolyse aesculin and arbutin. In addition, A. jandaei can be segregated from Aeromonas caviae and Aeromonas media by its production of gas from glucose and its positive response to Voges–Proskauer and gluconate oxidation tests. A. jandaei and Aeromonas schubertii can be separated on the basis of the negative responses displayed by the latter for the production of indole, acid from D-mannitol and gas from glucose. The key reactions that differentiate A. jandaei from phenotypically related species and reference strains of mesophilic Aeromonas species are detailed in Table 3. It is worth noting that Aeromonas culicicola and A. jandaei cannot be differentiated on the basis of the phenotypic profile reported recently by Pidiyar et al. (2002).
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; Abbott et al., 1992). In fact, the present study has demonstrated clearly that one of these previously identified A. veronii biogroup sobria isolates, CECT 4910, is a bona fide A. jandaei strain. Thus, such misidentifications could account for the scanty reports on A. jandaei in relation to human infectious diseases (Janda & Abbott, 1998). Moreover, the prevalence of A. jandaei in aquatic environments (fresh water and fish) is reported for the first time, as only one environmental strain, CECT 4231, has so far been isolated, from a prawn (Carnahan et al., 1991a). It is worth noting that environmental A. jandaei strains present LD50 values for mice similar to those reported for clinical A. jandaei strains (Supplementary Table A), and they can therefore be classified into the ‘high’ (LD50 <107·0 c.f.u.) or ‘moderate’ (LD50 107·0–107·5 c.f.u.) virulence categories described previously by Janda & Kokka (1991). Furthermore, nearly all A. jandaei strains have been able to degrade elastin, elastolytic activity currently being related to pathogenic significance in Aeromonas (Hsu et al., 1981). Thus, the clinical significance of the species A. jandaei and its importance in public health issues need to be reviewed in the light of the present findings.
Emended description of Aeromonas jandaei Carnahan et al. 1992
Gram-negative, straight rods that are motile by a single polar flagellum. Colonies develop within 24 h at 28 °C on TSA (Oxoid) and are not pigmented. No brown water-soluble pigment is produced. Growth occurs on MacConkey agar and on TCBS agar (Oxoid). Chemo-organotrophic, with both oxidative and fermentative metabolism. Acid and gas are produced from glucose. Kovacs' cytochrome oxidase- and catalase-positive. Reduces nitrate to nitrite. Does not swarm on solid media (1·5 % agar, w/v) and is resistant to vibriostatic agent O/129 (150 µg). Growth occurs in the presence of 0–3 % (w/v) NaCl, at temperatures between 4 and 42 °C and under alkaline (pH 8·5) conditions. All strains produce H2S from L-cysteine. Positive for indole, Moeller's arginine dihydrolase, Thornley's arginine, gluconate oxidation and Voges–Proskauer test but negative for Moeller's ornithine and glutamine decarboxylases. All strains produce acid from fructose, D-galactose, glycerol, D-mannose, D-mannitol, D-ribose and D-trehalose. None of the strains produces acid from adonitol, D-amygdalin, D-arabinose, L-arabinose, arbutin, dulcitol, 2-deoxy-D-glucose, myo-inositol, lactose, D-melibiose, D-raffinose, D-rhamnose, salicin, D-sorbitol, L-sorbose, xylitol or xylose. All strains use the following substrates as sole carbon and energy sources: N-acetylglucosamine, fumarate, D-gluconate, L-glutamate, L-glutamine, malate (alkalinization), L-proline and succinate. None of the strains uses trans-aconitate, adenine, L-alanine, 
-aminobutyrate, L-arabinose, L-arginine, L-asparagine, L-aspartate, benzoate, L-carnosine, L-citrulline, L-cysteine, D-galacturonate, D-glucuronate, glutarate, glutathione, glycine, guanine, L-isoleucine, L-lactate, L-leucine, L-lysine, maleate (alkalinization), malonate (alkalinization), L-methionine, mucate, L-ornithine, L-phenylalanine, propionate, putrescine, sarcosine, L-tartrate, L-threonine, L-tryptophan, L-tyrosine, L-valine or xanthine. Strains hydrolyse casein and gelatin but not alginate, arbutin or aesculin. All strains display amylase and lecithinase activities and excrete -haemolysins against human red blood cells. All strains are resistant to ampicillin and penicillin but sensitive to amikacin, gentamicin, tetracycline and tobramycin (Carnahan et al., 1991a; Esteve 1995). Additional characteristics that vary among strains are shown in Table 2. The DNA G+C content ranges from 58·1 to 61·1 mol%, as determined by the Tm method.
Isolated from clinical samples, fresh water, prawns and eels (Anguilla anguilla). Mostly virulent for eels and mice; the latter animal model is currently used to assess pathogenic significance for humans.
The type strain is ATCC 49568T (=CECT 4228T); it presents all of the properties given above for the species. In addition, it is positive for Moeller's lysine decarboxylase, produces acid from maltose, hydrolyses elastin, SDS and Tween 80 and uses acetate, citrate and L-serine (Table 2). However, it is negative for acid production from sucrose and D-cellobiose, does not grow at pH 4·5 and does not use DL-glycerate, L-histidine or D-glucosamine. Isolated from faeces. The DNA G+C content of the type strain is 58·8 mol%.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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