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Int J Syst Evol Microbiol 56 (2006), 1953-1957; DOI  10.1099/ijs.0.64355-0
© 2006 International Union of Microbiological Societies

Reclassification of Pseudomonas beijerinckii Hof 1935 as Chromohalobacter beijerinckii comb. nov., and emended description of the species

Janina Peçonek1, Claudia Gruber2, Virginia Gallego3, Antonio Ventosa3, Hans-Jürgen Busse4, Peter Kämpfer5, Christian Radax6 and Helga Stan-Lotter2

1 Warsaw Agricultural University, Faculty of Veterinary Medicine, Department of Food Hygiene and Public Health, 02-776 Warsaw, Poland
2 University of Salzburg, Division of Molecular Biology, Department of Microbiology, Billrothstr. 11, A-5020 Salzburg, Austria
3 Departamento de Microbiologia y Parasitologia, Facultad de Farmacia, Universidad de Sevilla, E-41012 Sevilla, Spain
4 Institut für Bakteriologie, Mykologie und Hygiene, Veterinärmedizinische Universität, Veterinärplatz 1, A-1210 Vienna, Austria
5 Institut für Angewandte Mikrobiologie, Justus-Liebig Universität Giessen, IFZ-Heinrich-Buff-Ring 26–32, D-35392 Giessen, Germany
6 Dr-Petter-Str. 20, A-5020 Salzburg, Austria

Correspondence
Helga Stan-Lotter
helga.stan-lotter{at}sbg.ac.at


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Pseudomonas beijerinckii (type strain DSM 7218T=ATCC 19372T=NCIMB 9041T) was isolated from salted beans and was first described by Hof in 1935. 16S rRNA gene sequence comparisons demonstrated its close relatedness (>97–99 %) to species of the genus Chromohalobacter. A recent isolate from salted herrings originating from the Baltic Sea, strain 3b, also clustered phylogenetically within this genus. Phenotypic features, substrate utilization, fatty acid profile, quinone and polar lipid composition and whole-cell protein patterns supported the similarity of strain 3b to P. beijerinckii DSM 7218T and confirmed its relatedness to members of the genus Chromohalobacter. The G+C content of the DNA from strain 3b and P. beijerinckii DSM 7218T was 60.4 and 60.7 mol%, respectively. DNA–DNA hybridization data showed that the two strains represent the same species, but are separated from Chromohalobacter canadensis, the closest species from a phylogenetic point of view. Therefore, the reclassification of Pseudomonas beijerinckii as Chromohalobacter beijerinckii comb. nov. (type strain DSM 7218T=ATCC 19372T=NCIMB 9041T) is proposed. The species description has been emended considering the new data on both the type strain and strain 3b.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain 3b is AM048787.


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The type strain of Pseudomonas beijerinckii was isolated during studies on the microbiota of salted beans and other food by Hof (1935)Go. At that time, great astonishment was still expressed about the profusion of live bacteria and yeasts in these essentially home-prepared and wholesome foods, whose salt concentrations varied widely. Although initially the focus was on the striking purple discoloration of salted beans thought to be caused by motile Gram-negative bacteria, which were named P. beijerinckii, studies showed that pigment production was variable and dependent on the growth medium. Anzai et al. (2000)Go, Quillaguamán et al. (2004)Go and Arahal & Ventosa (2005)Go suggested that, based on 16S rRNA gene sequences, P. beijerinckii might be transferred to the genus Chromohalobacter, proposed by Ventosa et al. (1989)Go to accommodate halophilic, rod-shaped, motile, Gram-negative isolates originating from the Dead Sea or marine salterns. The genus Chromohalobacter constitutes a phylogenetically coherent group (Arahal et al., 2002Go) and includes five species at the time of writing, Chromohalobacter marismortui (the type species) (Ventosa et al., 1989Go), C. canadensis, C. israelensis (Arahal et al., 2001aGo), C. salexigens (Arahal et al., 2001bGo) and C. sarecensis (Quillaguamán et al., 2004Go).

Recently, a Gram-negative, motile, halophilic strain, 3b, was isolated from salted herrings of the Baltic Sea (Beutling & Peçonek, 1995Go; Peçonek & Beutling, 1995Go). In this study, we compared strain 3b with P. beijerinckii DSM 7218T and examined the taxonomic position of both strains in more detail. The results indicated that the two strains belong to the same species and should be included in the genus Chromohalobacter.

For most experiments, strains were cultured at 30 °C on complex medium containing 8 or 10 % NaCl (DSM medium 593) or up to 25 % NaCl (Larsen, 1981Go). Phenotypic characteristics, including morphological, physiological, biochemical and nutritional features, were determined as described by Ventosa et al. (1982)Go and Quesada et al. (1984)Go.

Cells of strain 3b and P. beijerinckii DSM 7218T were Gram-negative, motile small rods, occurring singly. On solid complex medium (Larsen, 1981Go) with 10 % NaCl, colonies appeared slightly yellowish, opaque and circular, and were about 3 mm in diameter following 72 h of growth at 30 °C. They were able to grow in media containing 0.35–25 % NaCl, showing optimal growth at 8–10 % (w/v) NaCl. They were obligately aerobic. Other phenotypic characteristics are listed in the emended species description and in Table 1Go.


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  		Table 1. Phenotypic features that differentiate [P.] beijerinckii from other Chromohalobacter species

Strains: 1, [P.] beijerinckii DSM 7218T and strain 3b (strains gave identical results); 2, C. salexigens DSM 3043T; 3, C. israelensis ATCC 43985T; 4, C. canadensis ATCC 43984T; 5, C. marismortui ATCC 17056T; 6, C. sarecensis CCUG 47987T. Data were taken from Arahal et al. (2001aGo, bGo), Quillaguamán et al. (2004)Go and this study. ND, No data available.

 
The 16S rRNA-encoding gene of strain 3b was analysed as described by Stan-Lotter et al. (2002)Go, except that bacterial primers E27F and E1492R (DeLong, 1992Go) were used. The resulting 16S rRNA gene sequence consisted of 1507 nucleotides. Alignment of 16S rRNA gene sequences was carried out with the ARB software program (Ludwig et al., 1998Go, 2004Go). Phylogenetic trees were inferred by using three tree-making algorithms, maximum-parsimony, neighbour-joining (Saitou & Nei, 1987Go) and maximum-likelihood. Base-frequency filters were applied in the sequence comparison analysis. In all trees examined, P. beijerinckii DSM 7218T and strain 3b grouped together, being located in a separate branch within the species of the genus Chromohalobacter (Fig. 1Go). Sequence similarities were determined in a FASTA search (Pearson & Lipman, 1988Go) and showed that the sequence of strain 3b was 99.3 % similar to that of P. beijerinckii ATCC 19372T and 99.0, 97.4 and 96.7 % similar, respectively, to sequences of C. canadensis ATCC 43985T, C. marismortui ATCC 17056T and C. israelensis ATCC 43985T. Our phylogenetic analysis clearly indicates that strain 3b is closely related to the species P. beijerinckii.


Figure 1
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  		Fig. 1. Phylogenetic tree based on 16S rRNA gene sequence comparison showing the position of the type strain of P. beijerinckii, strain 3b and members of the genera Chromohalobacter and Halomonas. Cobetia marina ATCC 25374T was used as outgroup. The tree was obtained using the maximum-parsimony method of analysis of 16S rRNA gene sequences. Bootstrap values >=70 % are indicated at branch-points. Bar, 1 % sequence divergence.

 
DNA–DNA hybridization experiments were carried out by the DSMZ Identification Service as described previously (Stan-Lotter et al., 2002Go), using the thermal renaturation method of De Ley et al. (1970)Go with modifications by Huß et al. (1983)Go. Since the similarity of the 16S rRNA gene sequences between strain 3b, P. beijerinckii DSM 7218T and C. canadensis DSM 6769T was >=99 %, they were subjected to DNA–DNA hybridization experiments. The level of DNA–DNA relatedness between P. beijerinckii DSM 7218T and strain 3b was 92.6 and 94.3 % (two experiments); relatedness between P. beijerinckii DSM 7218T and C. canadensis DSM 6769T was 47.0 % and relatedness between strain 3b and C. canadensis DSM 6769T was 54.7 %. These data indicated that P. beijerinckii DSM 7218T and C. canadensis DSM 6769T do not belong to the same species, since DNA relatedness values <70 % have been suggested to justify designation to different species (Wayne et al., 1987Go); on the other hand, they showed that strain 3b is a member of the species P. beijerinckii.

In order to compare strain 3b further with P. beijerinckii DSM 7218T, the two strains were subjected to analyses of their fatty acid and polar lipid profiles and quinone systems. For reference, C. marismortui DSM 6770T was also included. Fatty acids were analysed as described by Kämpfer & Kroppenstedt (1996)Go, but TSA was supplemented with 10 % NaCl (w/v). The fatty acid profile of C. marismortui DSM 6770T (Table 2Go) was similar to that reported for this species by Labrenz et al. (2003)Go, although the relative amounts of C16 : 1 and C19 : 0 cyclo were significantly different. This variation might be explained if different NaCl concentrations were employed in the growth medium, which have been reported to influence the relative amount of certain fatty acids of Chromohalobacter species (Mutnuri et al., 2005Go; Vargas et al., 2005Go). The fatty acid profiles of P. beijerinckii DSM 7218T and strain 3b were similar (Table 2Go); both contained predominantly the single hydroxy acid C12 : 0 3-OH, C16 : 0, C18 : 1{omega}7c and C19 : 0 cyclo {omega}8c. Differences in the amounts of C16 : 0, C17 : 0 cyclo and C18 : 1{omega}7c distinguished the two strains from C. marismortui DSM 6770T. For quinone and polar lipid analysis, cells were grown on PYE medium (Busse et al., 2005Go) supplemented with 9 % NaCl (w/v). The content of respiratory quinones was determined as described previously (Tindall, 1990Go; Altenburger et al., 1996Go). The predominant quinone was ubiquinone Q-9 in C. marismortui DSM 6770T (98.6 %), P. beijerinckii DSM 7218T (95.9 %) and strain 3b (97.5 %); in addition, Q-8 was present in the three strains in smaller amounts (1.4, 4.1 and 2.5 %, respectively). This quinone system is in accordance with the characteristics of other genera of the family Halomonadaceae (Labrenz et al., 2003Go). The polar lipids of C. marismortui DSM 6770T, P. beijerinckii DSM 7218T (Fig. 2Go) and strain 3b were virtually identical, showing only quantitative differences. Diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine and two unknown phospholipids were present in major to moderate amounts. Moderate amounts of another unknown phospholipid were detected in P. beijerinckii DSM 7218T and strain 3b, which was found in only minor amounts in C. marismortui DSM 6770T. Minor to trace amounts of four unknown aminolipids, two unknown phospholipids and an unknown aminophospholipid were detected in all three strains. These similarities provide additional evidence that all three strains are members of a single genus.


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  		Table 2. Fatty acid composition of strain 3b, P. beijerinckii DSM 7218T and C. marismortui DSM 6770T

Values are percentages of total fatty acids. ND, Not detected.

 

Figure 2
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  		Fig. 2. Polar lipid profile of P. beijerinckii DSM 7218T following two-dimensional TLC and detection with molybdatophosphoric acid. Abbreviations: PE, phosphatidylethanolamine; PG,phosphatidylglycerol; DPG, diphosphatidylglycerol; PL1–5, unknown phospholipids; AL1–4, unknown aminolipids; APL1, unknown aminophospholipid.

 
Whole-cell protein patterns, following separation by SDS-PAGE (Stan-Lotter et al., 2002Go), were prepared from strain 3b, P. beijerinckii DSM 7218T, C. canadensis DSM 6769T, C. marismortui DSM 6770T and C. israelensis DSM 6768T. The protein patterns of strain 3b and P. beijerinckii DSM 7218T were almost identical; other strains had dissimilar patterns, which differed in the location and intensity of numerous protein bands (data not shown).

Our data clearly demonstrate that P. beijerinckii DSM 7218T and strain 3b are members of a single species and they support the suggestions of Anzai et al. (2000)Go, Quillaguamán et al. (2004)Go and Arahal & Ventosa (2005)Go that P. beijerinckii should be reclassified as a species of Chromohalobacter. Hence, we here propose assignment of P. beijerinckii to the genus Chromohalobacter as Chromohalobacter beijerinckii comb. nov., and the description of this species is emended on the basis of new data.

Description of Chromohalobacter beijerinckii comb. nov.
Basonym: Pseudomonas beijerinckii Hof 1935Go.

The previous description (Haynes & Burkholder, 1957Go) is emended with data for strains 3b and DSM 7218T. Cells are single, Gram-negative, motile rods, 0.4–0.6x1.8–2.5 µm. On solid complex medium containing 10 % NaCl, colonies are light yellow, opaque, circular and 3 mm in diameter. Growth occurs in media containing 0.35–25 % (w/v) NaCl; optimum is 8–10 % (w/v) NaCl. No growth is observed in the absence of NaCl. Growth occurs in liquid media containing 10 % NaCl from pH 4.5 to 8 (optimum is pH 7.5) and between 4 and 42 °C; the optimum temperature is 30 °C. Produces acid from glucose, xylose, galactose and arabinose but not from fructose, lactose, maltose, sucrose, trehalose, glycerol or mannitol. Reduces nitrate to nitrite. Nitrite is not reduced. Methyl red and Simmons' citrate tests are positive. Indole is not produced. Voges–Proskauer test (acetoin) is negative. beta-Galactosidase, H2S production and lysine, arginine and ornithine decarboxylase tests are negative. Starch, gelatin, casein, Tween 80 and aesculin are not hydrolysed. Urease and phosphatase are not produced. Catalase and oxidase are present. Predominant fatty acids are C16 : 0, C19 : 0 cyclo {omega}8c and C18 : 1{omega}7c; C17 : 0 cyclo and C12 : 0 3-OH are present in smaller amounts. Diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine and two unknown phospholipids are major to moderate compounds in the polar lipid profile; additionally, minor to trace amounts of four unknown aminolipids, three unknown phospholipids and an unknown aminophospholipid are detectable. The quinone system consists of the major compound Q-9 (>95 %) and small amounts of Q-8. The G+C content of the DNA is 60.4–60.7 mol%.

The type strain, DSM 7218T (=ATCC 19372T=NCIMB 9041T) was isolated from salted beans; its G+C content is 60.7 mol%. Another strain, strain 3b, was isolated from salted herring of the Baltic Sea.


   ACKNOWLEDGEMENTS
 
This work was supported partially by FWF project P16260 (to H. S.-L.) and by the Department of International Relations, University of Salzburg. We thank Dr Peter Schumann, DSMZ, Braunschweig, Germany, for determination of DNA–DNA relatedness.


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