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Laboratori de Microbiologia, Facultat de Farmacia, Universitat de Barcelona, Av. Joan XIII s/n, 08028 Barcelona, Spain
Correspondence
Jesús Guinea
jguinea{at}farmacia.far.ub.es
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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9c, 16 : 17c and 17 : 18c. 16S rRNA gene sequence analysis confirmed that the strains isolated belonged to the genus Psychrobacter. The results of the study assigned five isolates to P. immobilis, three isolates to P. glacincola and three isolates to novel Psychrobacter species. The names Psychrobacter luti sp. nov. (type strain NF11T=LMG 21276T= CECT 5885T) and Psychrobacter fozii sp. nov. (type strain NF23T=LMG 21280T =CECT 5889T) are proposed for these organisms.
Detailed physiological and biochemical properties and fatty acid compositions of the Antarctic isolates, transformation assay results and DNA–DNA hybridization results are available as supplementary material in IJSEM Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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to accommodate a group of non-motile, oxidase-positive, non-pigmented, chiefly psychrotolerant, Gram-negative rods or coccobacilli isolated from the skin of fish and chickens and from various processed foods (Juni, 1991). These strains were referred to as ‘Moraxella-like’ organisms (Shaw & Shewan, 1968) and the strains that were competent for genetic transformation (Juni & Heym, 1980) were grouped together as members of the genus Psychrobacter (Juni & Heym, 1986) which, at present, belongs to the family Moraxellaceae (Rossau et al., 1991).
In the description of the genus Psychrobacter, Juni & Heym (1986) indicated the isolation of Psychrobacter organisms from a variety of sources including fish, poultry, meat products, clinical sources and sea water and also as contaminants on complex media. After the description of the first species of this genus, Psychrobacter immobilis, several species isolated from natural environments have been described from Antarctic ornithogenic soils, sea ice and krill, deep-sea environments and sea water of the Pacific Ocean, internal tissues of an ascidian collected in the Indian Ocean and a bioaerosol originating from pigeon faeces (Bowman et al., 1996, 1997; Maruyama et al., 2000; Denner et al., 2001; Kämpfer et al., 2002; Romanenko et al., 2002). It is evident that cold environments constitute an ecological niche for Psychrobacter organisms and Antarctic environments are a source of Psychrobacter bacteria.
Several Gram-negative, oxidase-positive, non-motile, coccoid bacteria were isolated from samples collected in the South Shetland Islands (Antarctica) by a Spanish scientific expedition during the Antarctic summer of 1987–1988. These Antarctic isolates were assigned to the genus Psychrobacter. In this study, we establish the taxonomic position of these bacteria by using phenotypic, genotypic, chemotaxonomic and phylogenetic analyses. The results obtained enabled us to allocate some of them in known species, P. immobilis and Psychrobacter glacincola, and to describe two novel species, Psychrobacter luti sp. nov. and Psychrobacter fozii sp. nov.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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. Strains NF1, NF7, NF8 and NF11T were isolated from mud collected in the inlet Admiralty Bay (King George Island, South Shetland Islands), at the bottom of a glacier that is covered at high water. Strains NF18, NF19, NF20, EN1, EN2 and EN4 were isolated from sediment collected in Johnson's Dock (Livingston Island, South Shetland Islands). Strain NF23T was isolated from water collected in Johnson's Dock.
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Morphology.
Cell size and morphology were determined by scanning (Hitachi model S 3200) and transmission (Philips model 301) electron microscope observations of cells grown in trypticase soy broth (TSB; ADSA) at 15 °C. Motility was tested by using phase-contrast microscopy (Olympus model CHS).
Physiological and biochemical characteristics.
Oxidase, catalase, nitrate reduction, hydrolysis of lecithin, aesculin, gelatin, starch, DNA, casein and Tween 80, pH and temperature ranges for growth, sodium requirement, salt tolerance and susceptibility to antibiotics were determined as described by Bozal et al. (2002). Acid production from carbohydrates and carbon- and energy-source utilization tests were performed as described by Bowman et al. (1996). Urease and phenylalanine deaminase activity were determined following Cowan & Steel (1993). Tolerance to 5 % (w/v) bile salts (Oxoid) was tested on nutrient agar (ADSA).
API galleries (API 20E, API 20NE, ATB 32GN, API 20B, API ZYM; bioMérieux) were used to test additional biochemical characteristics and were prepared according to the manufacturer's instructions, except that the API tests were incubated for 5 days at 15 °C.
Gram staining was performed according to Hucker & Conn (1923) and was confirmed by the L-alanine aminopeptidase assay (Manafi & Kneifel, 1990; Hernandez Molina et al., 1991). Capsule staining was performed following the methods of Cowan & Steel (1993).
Determination of 2-keto-3-deoxyoctanoic acid (KDO) and LPS.
2-Keto-3-deoxyoctanoic acid (KDO) in LPS was determined according to protocols of Hanson & Phillips (1981), using cell-wall preparations obtained as described by Work (1971). LPS was obtained from whole-cell lysates using the methods of Hitchcock & Brown (1983) and Mandatori & Penner (1989). SDS-PAGE of whole-cell lysates was performed by the procedure of Sambrook et al. (1989) in a MiniProtean II electrophoresis cell (Bio-Rad) by using 12 % separation gels. Gels were silver-stained according to the method of Hitchcock & Brown (1983).
Transformation assay.
Crude DNA samples of bacterial isolates, Moraxella nonliquefaciens CECT 465T and Moraxella bovis CECT 468T were prepared and assayed for their ability to transform a hypoxanthine- and thiamin-requiring mutant of P. immobilis ATCC 43117 to prototrophy, according to the transformation assay for psychrobacters described by Juni & Heym (1980).
Fatty acid composition.
Fatty acids were prepared from 40 mg wet cell material harvested from a culture on TSB agar (30 g TSB, 15 g agar; BBL) incubated for 5 days at 15 °C. Whole-cell fatty acids were determined as described by Bozal et al. (2002).
Determination of DNA base composition.
DNA was extracted from strains and purified by the method of Marmur (1961). The G+C content was determined as described by Bozal et al. (2002).
DNA–DNA hybridization and phylogenetic analysis.
Genomic DNAs of bacterial strains were prepared by the procedure of Wilson (1987). DNA–DNA relatedness was measured fluorometrically by using the microplate hybridization method (Ezaki et al., 1989). 16S rDNA sequences for the Antarctic Psychrobacter strains were determined and phylogenetic analyses carried out as described by Bozal et al. (2002).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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a, c, e) and non-spore-forming. Diploforms were common. These strains formed non-pigmented colonies on TSA agar incubated at 15 °C. Colonies of NF1, NF7, NF8, NF23, EN1, EN2 and EN4 were circular, smooth, slightly convex and bright with a diameter of 2–4 mm, whereas colonies of NF11T, NF18, NF19 and NF20 were smooth, opaque, non-circular and spread little throughout the growth medium, with similar dimensions. Neither diffusible pigments nor bioluminescence were observed. The cells of all bacterial isolates presented capsules and were about 0·4–1·8 by 0·4–0·8 µm in size. The strains were moderately halophilic and tolerated NaCl levels of about 9·5–12·5 %. Strains NF1 and EN4 required Na+ at a concentration of 17 mM [0·1 % (w/v) NaCl]. The pH range for growth was 6–9·5 and the growth temperature range was 4–30 °C for all the strains isolated except NF1 and NF20, which grew at 4–25 °C. Bile salts (5 %) were not tolerated by the isolates.
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Gram stain tended to be retained in all the strains. The presence of a Gram-negative cell-wall structure was demonstrated by electron microscopy examinations of ultrathin sections (Fig. 1b, d, f
) and the presence of KDO and LPS. Except for strains NF7 and NF8, all isolates possessed L-alanine aminopeptidase, again indicating their Gram-negative character.
On the basis of the standard bacteriological characteristics (Gram-negative, oxidase-positive, coccoid morphology, lack of motility, growth a 4 °C, considerable halotolerance and strictly oxidative metabolism), the Antarctic bacterial isolates can be assigned to the genus Psychrobacter (Juni, 1991). Differences between strains NF11T, EN4 and NF23T and known Psychrobacter species are shown in Table 2.
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) confirmed unequivocally that the isolates were members of the genus Psychrobacter (Juni, & Heym, 1986; Juni, 1991). The results of the transformation assay are shown in Fig. A, available as supplementary material in IJSEM Online.
Cellular fatty acid composition
The results of the fatty acid analysis are summarized in Table B (available as supplementary material in IJSEM Online). Whole-cell fatty acid profiles were found to be similar to those of species of genus Psychrobacter, with 18 : 19c, 17 : 18c and 16 : 17c as the predominant components. The unsaturated fatty acid 18 : 19c (oleic acid) accounted for 41–63 % of the total content, as reported for P. immobilis (Moss et al., 1988), Psychrobacter frigidicola (Bowman et al., 1996), P. glacincola (Bowman et al., 1997), Psychrobacter pacificensis (Maruyama et al., 2000), Psychrobacter proteolyticus (Denner et al., 2001), Psychrobacter faecalis (Kämpfer et al., 2002), Psychrobacter submarinus and Psychrobacter marincola (Romanenko et al., 2002). The fatty acid profiles of strains NF23T and EN4 presented some differences with respect to the other isolates. These strains contained higher levels of 12 : 0 3-OH and 10 : 0 and less than half of the total content was oleic acid. The predominant components of the novel isolates NF11T, EN4 and NF23T (with respective contents in parentheses) were 10 : 0 (2·2, 5·9 and 5·8 %), 12 : 0 3-OH (2·4, 6·5 and 7·1 %), 16 : 17c (16, 23·1 and 21 %), 16 : 0 (1·4, 2·1 and 2·3 %), 17 : 18c (9·7, 8·8 and 12·6 %) and 18 : 19c (60·1, 45 and 41·3 %).
DNA base composition and DNA–DNA hybridization
The DNA G+C contents of the Antarctic isolates were 44 (NF23T), 45 (NF7, NF8, NF11T, NF18 and NF19), 46 (NF1, EN1, EN2 and EN4) and 47 (NF20) mol%, which agree with the range described for the genus Psychrobacter (44–46 mol%; Juni, 1991). Levels of DNA–DNA relatedness among the strains studied are shown in Table C (available as supplementary material in IJSEM Online). Strains EN1 and EN2 shared 98 % DNA–DNA reassociation, clearly above the level of 70 % accepted as the limit for species relatedness (Wayne et al., 1987). Other strain groups were defined with similarities above 70 %: NF7 and NF8; NF18, NF19 and NF20; and EN4 and NF23T. The DNA relatedness of NF7 and NF8 with NF1 was 57–59 %, whereas NF11T and strains EN4 and NF23T showed relatedness values of 30–40 % with respect to the other isolates. Relatedness at the borderline of species level was found between strains EN1 and EN2 and strains NF18, NF19 and NF20, showing relatedness values between 63 and 68 %. The latter group shared DNA relatedness above 83 % with P. immobilis LMG 7203T, which places these strains within this species. EN1 and EN2 showed relatedness values of 63–70 % to P. immobilis LMG 7203T. The phenotypic traits of isolates EN1 and EN2, such as the capacity to produce acid aerobically from some carbohydrates, suggests that EN1 and EN2 also belong to P. immobilis. The loosely related groups strain NF1 and strains NF7 and NF8 have common biochemical and physiological characteristics that place these isolates in the same species. The highest DNA relatedness of the latter three isolates to known Psychrobacter species was to P. glacincola LMG 21282T (51–57 %). No significant similarities were found between the Psychrobacter type strains and isolate NF11T or the group constituted by EN4 and NF23T. The highest DNA relatedness of these isolates was found to P. immobilis LMG 7203T (36–39 %).
Phylogeny
16S rRNA phylogenetic studies confirmed that strains NF1, NF7, NF11T and NF23T are members of the genus Psychrobacter (Fig. 2). Similarities significant for possible species relatedness (over 97 %; Stackebrandt & Goebel, 1994) were found between the four strains, as follows: strains NF11T–NF23T (99·1 %), NF1–NF7 (99·0 %), NF7–NF23T (98·9 %), NF1–NF11T (98·8 %), NF7–NF11T (98·5 %) and NF1–NF23T (98·3 %). The similarities shown by NF1 and NF7 to Psychrobacter type strains were respectively 98·9 and 99·0 % to P. glacincola LMG 21282T, 97·8 and 98·8 % to P. immobilis LMG 7203T, 97·8 and 97·7 % to P. proteolyticus LMG 21313T and 97·8 and 97·4 % to P. faecalis DSM 14664T. Strain NF1 showed similarities of 97·3 % to P. submarinus DSM 14161T and 97·1 % to P. marincola DSM 14160T. The highest similarity of NF11T to a defined type strain was to P. glacincola LMG 21282T (98·4 %) followed by P. immobilis LMG 7203T (98·2 %), P. submarinus DSM 14161T (98·0 %) and P. proteolyticus LMG 21313T, P. marincola DSM 14160T and P. faecalis DSM 14664T (97·8 %). The relatedness values shown by NF23T were 99·0 % to P. immobilis LMG 7203T, 98·8 % to P. glacincola LMG 21282T, 98·2 % to P. proteolyticus LMG 21313T and 97·0 % to P. submarinus DSM 14161T and P. marincola DSM 14160T.
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Description of Psychrobacter luti sp. nov.
Psychrobacter luti (lut'i. L. masc. gen. n. luti of mud, referring to the isolation of strains from Antarctic glacier mud).
Cells are Gram-negative, non-motile, non-pigmented, non-spore-forming coccobacilli, 0·4–1·8 µm long and 0·4–0·6 µm wide. Growth occurs at 4–30 °C. Colonies on TSA are about 2 mm in diameter, smooth, opaque and non-circular, and spread little throughout the growth medium after 5 days at 15 °C. Able to grow in the absence of NaCl and can tolerate 9·5 % (w/v) NaCl. Strictly aerobic; oxidase and catalase tests are positive. Acid is not produced from carbohydrates. Cells are able to reduce nitrate to nitrite. Urease and tryptophan deaminase are not produced. Positive in the following biochemical tests: phenylalanine deaminase, alkaline phosphatase, esterase (C4), esterase lipase (C8), lipase (C14), leucine arylamidase and lecithinase. Positive for hydrolysis of casein and Tween 80. Growth occurs on L-histidine, L-proline, L-hydroxyproline, L-malic acid, sodium succinate, L-arginine, L-glutamine, Tween 80, DL-phenylalanine, putrescine, sodium acetate, L-ornithine, sodium citrate, 1-butanol and L-asparagine. The main cellular fatty acids are 18 : 19c, 16 : 17c and 17 : 18c. The G+C content of DNA of the type strain is 45 mol%.
The type strain, strain NF11T (=LMG 21276T =CECT 5885T), was isolated from muddy soil collected from the inlet Admiralty Bay on King George Island, South Shetland Islands, Antarctica.
Description of Psychrobacter fozii sp. nov.
Psychrobacter fozii (fo'zi.i. N.L. gen. n. fozii of Foz, named after Amadeo Foz, a Spanish physician who was an early pioneer in Spanish brucellosis).
Cells are Gram-negative, non-motile, non-pigmented, non-spore-forming coccobacilli, 0·4–1·8 µm long and 0·4–0·6 µm wide, and occur in pairs or in short chains. Growth occurs at 4–30 °C. Colonies on TSA are circular, smooth, slightly convex and bright with a diameter of 2–4 mm after 5 days at 15 °C. Halotolerant, able to grow in the presence of 10–12·5 % (w/v) NaCl. Strictly aerobic. Acid is not produced from carbohydrates. Oxidase, catalase and urease tests are positive. Nitrate reduction and tryptophan deaminase are negative. Positive in the following biochemical tests: alkaline phosphatase, esterase (C4), esterase lipase (C8) and leucine arylamidase. Growth occurs on ethanol, L-alanine, D-alanine, L-histidine, L-proline, L-hydroxyproline, L-malic acid, propionic acid, sodium succinate, sodium pyruvate, L-arginine, L-glutamine, Tween 80, DL-phenylalanine, L-asparagine and putrescine. The type strain also uses D-mannitol, laevulose, 1-butanol, sodium acetate and L-ornithine. The main cellular fatty acids are 18 : 19c, 16 : 17c and 17 : 18c. The G+C content of DNA is 44–46 mol%.
The type strain, strain NF23T (=LMG 21280T =CECT 5889T), was isolated from sediment collected in Johnson's Dock, Livingston Island, South Shetland Islands, Antarctica.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Bowman, J. P., Nichols, D. S. & McMeekin, T. A. (1997). Psychrobacter glacincola sp. nov., a halotolerant, psychrophilic bacterium isolated from Antarctic sea ice. Syst Appl Microbiol 20, 209–215.
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