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Department of Veterinary Microbiology, the Royal Veterinary and Agricultural University, Stigbøjlen 4, 1870 Frederiksberg C, Denmark
Correspondence
Henrik Christensen
hech{at}kvl.dk
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of strains Gerl. 236/81T, 146/S8/89T and B96/5 are AY216868–AY216870 and those for strains 94, 101 and 103 are AF487722–AF487724, respectively.
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TOPABSTRACTMAIN TEXTREFERENCES |
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). Accurate diagnosis of bacteria isolated from diseased pet birds is a prerequisite for disease treatment and prevention, in addition to health improvement. Especially with members of the Pasteurellaceae, identification has remained a problem, because many groups are weakly characterized or are at most classified as unnamed taxa. This might result in uncertain or misleading identification (Bisgaard, 1993; Christensen et al., 2002b, 2003b).
Twelve strains, all originating from psittacine bird species, were shown to represent a new taxon tentatively named Bisgaard taxon 33 on the basis of phenotypic characterization and ribotyping (Bisgaard et al., 1999). Ribotyping of selected strains showed that taxon 33 strains formed a separate cluster (Bisgaard et al., 1999). The original publication included isolates obtained from lesions of lungs, trachea, air sac, liver, spleen and eyes of parrots. Since this publication, 13 additional strains have been obtained and investigated and been found to be both phenotypically and genotypically similar to taxon 33.
The present study aimed at a final classification of Bisgaard taxon 33, with the proposal of a new genus within the Pasteurellaceae.
Phenotypic characterization
In addition to the 12 strains already characterized phenotypically, nine of which were ribotyped in the previous publication (Bisgaard et al., 1999), 13 further strains were phenotyped according to Bisgaard et al. (1991). The total number of strains investigated originated from parrots (15), budgerigars (7), parakeets (2) and a chicken. With the exception of a single isolate, all isolates were obtained from lesions, mostly from the respiratory tract or septicaemia. Isolates have so far only been obtained in European countries, including Belgium, Denmark and Germany.
Common phenotypic characteristics of the 25 strains classified with Bisgaard taxon 33 and proposed as Volucribacter gen. nov. included positive reactions for methyl red, nitrate, porphyrin and acid production without gas from (–)-D-ribose, (–)-D-fructose, (+)-D-galactose, (+)-D-glucose, (+)-D-mannose, sucrose and raffinose, whereas negative reactions were observed for symbiotic growth, urease, ornithine decarboxylase, 
-glucosidase (PNPG; 4-nitrophenyl -D-glucopyranoside) and fermentation of (–)-D-mannitol, (–)-D-sorbitol and trehalose. A full list of the 81 phenotypic characters investigated is given with the description of the genus.
Characters that are variable within the genus are listed with Table 1 and allow two biovars to be distinguished. Biovar 1, including 22 strains, is negative for the ONPG (o-nitrophenyl D-galactopyranoside) test and does not produce acid from (–)-L-fucose, maltose or dextrin, whereas biovar 2, including three strains, is positive for these characters.
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-galactosidase-positive variant of Volucribacter, while strain B96/5 represents an (+)-L-arabinose-, meso-inositol-, ONPG, maltose- and dextrin-positive variant. Finally, strain 64 can be regarded as a (+)-D-xylose-, meso-inositol-, lactose-, ONPG-, maltose-, melibiose-, dextrin- and -galactosidase-positive variant. The existence of two biovars indicated the existence of two species within Volucribacter, as also indicated by the lower 16S rRNA gene sequence similarities between the biovars than within them and the low degree of DNA–DNA hybridization (see below).
The phenotypic characters indicate that Volucribacter is a member of the Pasteurellaceae as defined by Olsen et al. (2004) and previously suggested by Bisgaard et al. (1999). Between two and four phenotypic characters separate the genus Volucribacter from other genera of the Pasteurellaceae (Table 2). Data for the other genera and genus-like groups of Pasteurellaceae were obtained from Angen et al. (1999) (Mannheimia), Mutters et al. (2004) (Pasteurella sensu stricto), Osawa & Stackebrandt (2004) (Lonepinella), Foster & Collins (2004) (Phocoenobacter), Kilian (2004) (Haemophilus sensu stricto), Christensen et al. (2003a) (Gallibacterium), Angen et al. (2003) (Histophilus somni) and Christensen & Bisgaard (2004) (Actinobacillus sensu stricto). Only differences in (–)-D-mannitol and -glucosidase separate taxon 33 from Gallibacterium. However, most isolates of Gallibacterium are 
-haemolytic and trehalose-positive, while taxon 33 is negative. At least three phenotypic characters separate taxon 33 from other existing genera containing avian taxa. Separation from possible candidates for new genera containing avian taxa, including Pasteurella sensu stricto of cluster 18 (Olsen et al., 2004), [Haemophilus] paragallinarum and the taxon 2 and 3 complex of Bisgaard, has to await separate investigations.
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). PCR amplification was performed as described by Vogel et al. (1997). Oligonucleotides for both PCR amplification and sequencing were synthesized according to sequences and 16S rRNA positions given by Dewhirst et al. (1989) and Paster & Dewhirst (1988). PCR-amplified fragments were purified on Microspin columns (Pharmacia Biotech) and cycle-sequenced (Thermo Sequenase fluorescent-labelled primer cycle-sequencing kit; Amersham) on an ALF sequencer (Pharmacia Biotech) using fluorescein-labelled primers.
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. Searches for 16S rRNA sequences were performed by FASTA and BLAST by use of the Wisconsin sequence analysis package (GCG, Madison). Pairwise comparisons for similarity were performed by BESTFIT (GCG). The four strains Gerl. 236/81T, 94, 101 and 103 of biovar 1 showed 99·2–99·9 % similarity, whereas the two strains B96/5 and 146/S8/89T of biovar 2 showed 99·9 % 16S rRNA similarity. The lowest similarity observed between biovar 1 and 2 strains was 98·8 %, between strains 94 and B96/5, while the highest similarity (99·5 %) was observed between strains 103 and 146/S8/89T. Strain Gerl. 236/81T showed 99·2–99·9 % similarity to biovar 1 strains and 99·4 % similarity to biovar 2 strains. Such high 16S rRNA similarity between species is not unusual for members of the Pasteurellaceae, where 16S rRNA similarities of 99·7 % between type strains of Pasteurella gallinarum and Pasteurella volantium, as well as between Actinobacillus lignieresii and Actinobacillus pleuropneumoniae, corresponded to 72 % DNA reassociation (Pohl et al., 1983; Mutters et al., 1985), and 99·6 % 16S rRNA similarity between the type strains of Actinobacillus suis and Actinobacillus equuli corresponded to 66 % DNA reassociation (Christensen et al., 2002a). The highest 16S rRNA similarity outside the genus Volucribacter was found to the type stain of Pasteurella avium (accession no. M75058; 94·5 %) for strain 101 and to strain 69 of Bisgaard taxon 34 (accession no. AY172731; 94·6 % similarity) for strain 94.
Phylogenetic analysis
The alignment was constructed by PILEUP (GCG) and included the region between Escherichia coli positions 64 and 1391 of rrnB, with 1283 positions left after removal of ambiguous positions and 184 distinct data patterns analysed. The alignment was in accordance with the secondary structure mask of Lane (1991). Maximum-likelihood analysis including bootstrap analysis was performed by fastDNAmL (Olsen et al., 1994) run on a Linux 7.2-compatible server with a transition/transversion ratio of 1·5. Parsimony and neighbour-joining analysis were performed by PHYLIP (Felsenstein, 1995).
The high 16S rRNA gene sequence similarity between the strains of taxon 33 proposed as Volucribacter was reflected in the phylogenetic comparison, where the representatives of the taxon formed a distinct monophyletic group supported by a bootstrap value of 99 % (Fig. 1). The phylogenetic analysis shown in Fig. 1 was based on 16S rRNA gene sequences of type strains of the genera of Pasteurellaceae. The topology shown in Fig. 1 was identical when data were analysed by maximum-parsimony and neighbour-joining analysis. The distinct phylogenetic position of Volucribacter (Bisgaard taxon 33) with reference to all members of the family Pasteurellaceae has been shown previously (Christensen et al., 2003b). The genus was related to representatives of other members of the ‘avian’ cluster (Olsen et al., 2004), including members of Pasteurella sensu stricto (Mutters et al., 1989) isolated from birds, the new genus Gallibacterium (Christensen et al., 2003a), [Haemophilus] paragallinarum and taxa 2, 3 and 34 of Bisgaard (Christensen et al., 2003b). In conclusion, the proposed genus Volucribacter was unrelated to representatives of type species and 16S rRNA clusters (Olsen et al., 2004) of Pasteurellaceae.
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. The DNA reassociation between strains Gerl. 236/81T and 101 of biovar 1 was 94 % (Table 4). DNA reassociation between strain Gerl. 236/81T from biovar 1 and 146/S8/89T from biovar 2 was only 47 %, underlining the presence of two species. The DNA reassociation results published by Piechulla et al. (1985) were at most 24 % to other taxa investigated, as observed between Gerl. 236/81T and three strains of taxa 2 and 3 of Bisgaard. Only 6 % DNA reassociation was found between Gerl. 236/81T and the type strain of Pasteurella gallinarum. A value of 70 % DNA reassociation between strain Gerl. 236/81T and strain Gerlach 3348/80 (=F 219) of Gallibacterium was observed by Piechulla et al. (1985). This result was subsequently reinvestigated and found to be only 11 % (Christensen et al., 2003a). A value of 76 % DNA reassociation was found between Gerl. 236/81T and a V-factor-requiring strain, Sittich 1, obtained from a parakeet (Piechulla et al., 1985). Further information is unfortunately not available for this strain. A group of Pasteurella avium-like organisms obtained from the respiratory tract of psittacine birds was reported by Beichel (1986). The single isolate (103) included in the present investigation and meeting the phenotypic characters of taxon 33 showed DNA reassociation values between 24 and 30 % with Pasteurella multocida, Pasteurella stomatis, Pasteurella avium and Gallibacterium anatis and between 18 and 44 % with Bisgaard taxon 16 (Stenzel, 1992).
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Description of Volucribacter gen. nov.
Volucribacter (Vo.lu.cri.bac'ter. L. fem. n. volucris bird; N.L. masc. n. bacter rod; N.L. masc. n. Volucribacter rod-shaped bacterium of birds).
Gram-negative rods forming surface colonies on blood agar that are circular and slightly raised with an entire margin. The surface of the colonies is smooth, shiny and opaque with a greyish tinge. Colonies are 1·0–1·5 mm in diameter after aerobic incubation at 37 °C for 24 h. After incubation for 48 h, a diameter of 2·0 mm might be reached. The consistency is buttery and colonies do not adhere to the agar surface. Growth on bovine blood agar is not accompanied by haemolysis. A greenish colour is sometimes associated with heavy growth. (+)-D-Glucose is catabolized fermentatively in Hugh and Leifson's medium and porphyrin, methyl red (37 °C), nitrate reduction and alanine aminopeptidase tests are positive within 1–2 days. (–)-D-Fructose, (+)-D-glucose, (+)-D-mannose and sucrose are fermented within 1–2 days, while (–)-D-ribose, (+)-D-galactose and raffinose are positive after 3 or more days. The phosphatase test is positive, but weak reactions might occur. Within 14 days of incubation, motility at 37 and 22 °C is negative, and tests for symbiotic growth, growth on Simmons' citrate, malonate base, H2S formation in TSI, KCN growth, Voges–Proskauer at 37 °C, gas from nitrate, urease, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, phenylalanine deaminase, indole formation, gelatinase, hydrolysis of Tween 20 or 80, MacConkey growth, pigment, formation of gas from (+)-D-glucose, -fucosidase, -glucosidase, -glucuronidase, -mannosidase and -xylosidase are all negative. Acid is not formed from mucate, meso-erythritol, adonitol, (+)-D-arabitol, xylitol, (–)-L-xylose, dulcitol, (–)-D-mannitol, (–)-D-sorbitol, (+)-D-fucose, (+)-L-rhamnose, (–)-L-sorbose, trehalose, cellobiose, (+)-D-melezitose, (+)-D-glycogen, inulin, aesculin, amygdalin, arbutin, gentiobiose, salicin, (+)-D-turanose or N-methyl -glucosamide. Variable characters include catalase, oxidase, glycerol, (+)-L-arabinose, (–)-D-arabinose, (+)-D-xylose, meso-inositol, (–)-L-fucose, lactose, ONPG, maltose, (+)-D-melibiose, dextrin and -galactosidase. The bacteria have been isolated from parrots, budgerigars, parakeets and a chicken, mainly showing respiratory tract or septicaemic lesions. The type species is Volucribacter psittacicida.
Description of Volucribacter psittacicida sp. nov.
Volucribacter psittacicida (psit.ta.ci'ci.da. L. masc. n. psittacus the parrot; L. masc./fem. suffix n. -cida killer; N.L. masc. n. psittacicida killer of parrots).
Colony and cellular morphology and phenotypic reactions are identical to those given in the genus description. In addition, the species is positive or weakly positive in reactions for phosphatase. Late positive reactions are observed with glycerol, while negative reactions are observed with (+)-L-arabinose, (–)-D-arabinose, (+)-D-xylose, meso-inositol, (–)-L-fucose, lactose, maltose, (+)-D-melibiose, dextrin, -galactosidase and ONPG. Variable reactions are observed for catalase and oxidase. The species can be separated from V. amazonae by the lack of fermentation of meso-inositol, (–)-L-fucose, maltose and dextrin and the negative ONGP reaction. Plasmids were not found in the type strain (procedure reported by Christensen et al., 2003a).
The type strain is Gerl. 236/81T (=CCUG 47536T=DSM 15534T), obtained from a parakeet with septicaemia and received from H. Gerlach, Munich, Germany, in 1981. The characterization was based on 22 strains from three different countries representing isolates mostly obtained from lesions in parrots, budgerigar, parakeets and a chicken. The DNA G+C content of strain 103 was 39·9 mol%, while the genome mass was 1·4x109 Da (Stenzel, 1992). The G+C content of strain Gerl. 236/81T was 40·8 mol% and the genome mass 2·4x109 Da (Piechulla et al., 1985).
Description of Volucribacter amazonae sp. nov.
Volucribacter amazonae (a.ma.zo.na'e. N.L. gen. sing. n. amazonae of parrots of the genus Amazona).
Colony and cellular morphology and other phenotypic reactions are identical to those given in the genus description; in addition, the species is positive for catalase, phosphatase and ONPG and ferments meso-inositol, (–)-L-fucose, maltose and dextrin. Variable reactions are observed for production of acid from glycerol, (+)-L-arabinose, (–)-D-arabinose, (+)-D-xylose, lactose and (+)-D-melibiose and the -galactosidase test. The species can be separated from V. psittacicida by fermentation of meso-inositol, (–)-L-fucose, maltose and dextrin and positive reaction for ONPG.
Three strains of the species isolated from parrots and parakeet have been characterized. The type strain, 146/S8/89T (=CCUG 47537T=DSM 15535T), was originally isolated from an African grey parrot (Psittacus erithacus) with septicaemia by H. Gerlach, Munich, Germany, in 1989.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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Angen, Ø., Ahrens, P., Kuhnert, P., Christensen, H. & Mutters, R. (2003). Proposal of Histophilus somni gen. nov., sp. nov. for the three species incertae sedis ‘Haemophilus somnus’, ‘Haemophilus agni’ and ‘Histophilus ovis’. Int J Syst Evol Microbiol 53, 1449–1456.
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