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1 Institut für Mikrobiologie, Universität Innsbruck, Technikerstrasse 25, A-6020 Innsbruck, Austria
2 Deutsche Sammlung für Mikroorganismen und Zellkulturen, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
Correspondence
Rosa Margesin
rosa.margesin{at}uibk.ac.at
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-glucosidase, -galactosidase and -lactamase and degraded oil hydrocarbons. A distinct optimum temperature of 15 °C was observed for both protease production and oil hydrocarbon biodegradation. Analysis of 16S rDNA revealed that strain A37T represents a distinct taxon within Pedobacter. DNA from strain A37T showed only 19·7 % genetic relatedness to the DNA of Pedobacter piscium. The DNA G+C content was 43·4 mol%. Dominant fatty acids (51 %) were iso-15 : 0 2-OH and 16 : 1
7c. The strain is assigned to a novel Pedobacter species, for which the name Pedobacter cryoconitis sp. nov. is proposed, with A37T (=DSM 14825T=LMG 21415T) as the type strain.
The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of strain A37T is AJ438170.
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; Margesin et al. 2002a). A wide range of metabolic activities has been detected at low temperatures, including degradation of natural and xenobiotic organic compounds such as protein, cellulose, carbohydrates, lignin and aliphatic and aromatic hydrocarbons (Morita et al., 1997; Huston et al., 2000; Margesin et al., 2002b). Micro-organisms able to degrade oil hydrocarbons at low temperatures are useful for the bioremediation of contaminated cold environments (Bej et al., 2000; Margesin & Schinner, 2001; Yumoto et al., 2002).
Adaptation strategies with regard to growth, enzyme production and enzyme activity enable cold-adapted micro-organisms to compensate for the negative effects of low temperatures on biochemical reactions. These organisms can be isolated from permanently cold environments such as fresh and marine waters, snow, glacier and sea ice, polar and high-alpine soils, cold deserts and permafrost soils. An ideal habitat is cryoconite on glacier ice (Takeuchi et al., 2001; Margesin et al., 2002b), a dark mixture on the surface and in microcaverns of glaciers, consisting predominantly of organic debris (micro-organisms, pollen, plant and animal litter) and inorganic dust. Little is known of the microbial life in alpine cryoconite.
We isolated a facultatively psychrophilic representative of the genus Pedobacter from alpine glacier cryoconite and report the results of a phenotypic, genetic and phylogenetic examination. The strain degrades diesel oil and produces high yields of protease at low temperatures. The data obtained suggest that the isolate represents a novel species of the genus Pedobacter, and the name Pedobacter cryoconitis sp. nov. is proposed.
Cryoconite samples were collected in a ski area on the Stubaier Glacier in the Tyrolean Alps (Austria) at an altitude of 3000 m above sea level and microbial strains were isolated as described by Margesin et al. (2002b). Morphological and phenotypic properties of the strain were investigated by using standard procedures (Süßmuth et al., 1987). Aminopeptidase activity (Bactident; Merck) was tested to confirm classical Gram-staining. The biochemical profile was determined with API 20NE strips (bioMérieux) incubated at 10 and 20 °C for up to 4 days. Carbon assimilation was tested by using API 50CH strips (bioMérieux) incubated at 20 °C for up to 5 days. Sensitivity to antibiotics was determined with ATB G- and ATB G+ strips (bioMérieux) at 10 and 20 °C. Amylase, protease, lipase and -lactamase activities were tested on nutrient broth agar plates supplemented with starch or skimmed milk (2 g each compound l-1), tributyrin (5 ml l-1) or ampicillin (50 mg l-1). After 24–48 h at 10 °C, a positive reaction was observed when transparent zones around the colonies were visible directly or detected after precipitation or staining of the undegraded substrate. In the case of -lactamase activity, a positive reaction was indicated by growth in the presence of ampicillin.
Strain A37T isolated from alpine glacier cryoconite had all of the phenotypic characteristics of the genus Pedobacter (Steyn et al., 1998) (Table 1). The cells were Gram-negative, aerobic, rod-shaped (0·7–0·9 µm in diameter and 1·5–3·0 µm long), non-spore-forming, non-flagellated and motile by gliding. On R2A agar (composition given below), colonies were round, 2–4 mm in diameter, slightly convex, with entire margins, mucoid, motile by gliding and had a light-yellow non-fluorescent pigment. Activities of oxidase, catalase, DNase, amylase, -glucosidase, -galactosidase, protease (gelatin and casein) and -lactamase were present, while activities of arginine dihydrolase, urease, esterase lipase (C4) and tryptophan deaminase, nitrate reduction, H2S production from thiosulfate, indole production and growth on MacConkey agar were not detected.
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-gentiobiose, D-turanose, gluconate and 2-ketogluconate. Methyl 
-D-glucoside and inulin were assimilated to a lesser extent. Assimilation of amygdalin and N-acetylglucosamine was only noted after 8 days of incubation. The following carbohydrates were not assimilated: glycerol, erythritol, D-arabinose, ribose, L-xylose, adonitol, methyl -xyloside, L-sorbose, rhamnose, dulcitol, inositol, mannitol, sorbitol, methyl -D-mannoside, melezitose, xylitol, D-lyxose, D-tagatose, D-fucose, D-arabitol, L-arabitol, 5-ketogluconate, phenylacetate, citrate, malate, adipate and caprate. Thus, strain A37Tcan be distinguished from three Pedobacter species by its inability to assimilate rhamnose and from four Pedobacter species by its ability to assimilate glycogen, 2-ketogluconate and, to a lesser extent, inulin (Table 1
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The study of antibiotic susceptibility showed that strain A37T was sensitive to sulfamethoxazole, which is a characteristic feature of Pedobacter species, and also to doxycycline and clindamycin. Resistance was observed to a wide range of antibiotics: penicillins (penicillin, ampicillin, mezlocillin, oxacillin, amoxicillin), cephalosporins (cephalothin, cephotaxim, cephazolin, cephtazidim, cephamandole), other -lactams (aztreonam, imipenem), aminoglycosides (gentamicin, streptomycin), erythromycin, amikacin, chloramphenicol, tetracycline, fusidic acid and quinolones (ciprofloxacin, norfloxacin).
Analysis of fatty acid methyl esters was performed by GLC as described previously (Miller, 1982; Sasser, 1990). Dominant fatty acids (51 %) were iso-15 : 0 2-OH and 16 : 17c. The presence of significant amounts of these two fatty acids is characteristic of all representatives of the family Sphingobacteriaceae (Steyn et al., 1998).
Genomic DNA extraction, PCR-mediated amplification of the 16S rDNA, purification of PCR products and electrophoresis of sequence reactions were done as described previously (Rainey et al., 1996). The 16S rDNA sequence was aligned manually with published sequences from representatives of the Cytophaga–Flavobacterium–Bacteroides (CFB) group contained in the DSMZ database of 16S rDNA sequences. The ae2 editor (Maidak et al., 1999) was used to align the 16S rDNA sequence of strain A37T against sequences of Pedobacter type strains available from public databases. Pairwise evolutionary distances were computed using the correction of Jukes & Cantor (1969). The least-squares distance method of De Soete (1983) was used in the construction of the phylogenetic dendrogram from distance matrices. Bootstrap analyses were done as described by Felsenstein (1993).
The almost-complete 16S rDNA sequence of strain A37T, consisting of 1495 nt, was compared with sequences of members of the CFB group. Members of the genus Pedobacter were the closest phylogenetic neighbours. Binary similarity values ranged between 97·9 % (Pedobacter piscium DSM 11725T) and 90·3 % (Pedobacter saltans DSM 12145T). Similarly high values separated the type strains of Pedobacter heparinus (DSM 2366T) and Pedobacter africanus (DSM 12126T) (97·9 %). Distance matrix analyses placed strain A37T in a separate line of descent, showing no close relatedness to any of the type strains of Pedobacter (Fig. 1).
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. DNA–DNA hybridization was carried out as described by De Ley et al. (1970), with the modification described by Huß et al. (1983) and Escara & Hutton (1980), using a model 2600 spectrophotometer equipped with a Gilford model 2527-R thermoprogrammer and plotter. Renaturation rates were computed with the TRANSFER.BAS program (Jahnke, 1992). DNA from strain A37T showed only 19·7 % genetic relatedness to the DNA of P. piscium. Based on generally accepted criteria of the definition of genomic species (Wayne et al., 1987), strain A37T is assigned to a separate species.
The DNA G+C content for the genus Pedobacter ranges broadly from 36·9 mol% (reported for P. saltans) to 44·1 mol% (reported for P. africanus) (Steyn et al., 1998). The G+C content of the DNA of strain A37T was 43·4 mol%, determined after degradation of the DNA as described by Mesbah et al. (1989) and separation of the resulting nucleosides by HPLC as described by Tamaoka & Komagata (1984).
Strain A37T was routinely cultivated in the low-strength medium R2A, containing 0·05 % yeast extract, 0·05 % peptone, 0·05 % Casamino acids, 0·05 % glucose, 0·05 % starch, 0·03 % sodium pyruvate, 0·03 % K2HPO4 and 0·005 % MgSO4 (pH 7). This medium is suitable for the cultivation of micro-organisms from oligotrophic environmental habitats. Cultivation was done aerobically at 180 r.p.m. in 100-ml Erlenmeyer flasks containing 10 ml R2A medium with an initial cell density of 108 c.f.u. ml-1 and three replicates per treatment, unless indicated otherwise.
The pH tolerance (pH 5–10) for growth was determined after 48 h at 20 °C. The pH range for growth was 5–8, with optimum growth at pH 6–7.
The temperature tolerance for growth was examined at 1–30 °C in the absence and presence of oil hydrocarbons [2 g diesel oil l-1 (85·7 % C, density 820 g l-1)]. Cell density in cultures was determined from cell protein concentrations. Protein was measured according to Bradford (1976) after disintegration of cells by boiling in 0·1 M NaOH for 10 min (Chen & Skidmore, 1987). There was no interference of diesel oil with this method. Optical density measurements were not possible in the presence of hydrocarbons due to the formation of cell aggregates. The bacterium exhibited the properties of a facultative psychrophile (Morita, 1975), showing a growth temperature range of 1–25 °C and an optimum growth temperature of 20 °C after 24 h cultivation. After 48 h, comparable cell densities were detected over a cultivation temperature range of 10–25 °C. No growth occurred at 28 °C. Comparable cell densities were measured in cultures with and without diesel oil at all temperatures tested. Since the growth temperature range for strains of the genus Pedobacter is normally between 5 and 30 °C, and some strains of this genus may even grow at 37 °C (Steyn et al., 1998), strain A37T can be easily distinguished from other Pedobacter species by its inability to grow at 28 °C and its ability to grow well at 1 °C.
Another characteristic feature of strain A37T is the ability to degrade oil hydrocarbons, which has not yet been described for other Pedobacter species. The effect of temperature on hydrocarbon biodegradation was evaluated at 1–25 °C in the dark in R2A medium containing 2 g diesel oil l-1. After 1–8 days, the residual hydrocarbon content was measured in inoculated and in sterile flasks as described previously (Margesin & Schinner, 1997). Co-metabolic oil hydrocarbon biodegradation was calculated from the difference between hydrocarbon losses in the inoculated and sterile medium. Maximum biodegradation was observed at 15 °C; cultivation at this temperature resulted in decontamination of 53 % of the diesel oil added (2 g l-1) after 4 days. At lower temperatures, biodegradation was still remarkable (38–40 % at 5–10 °C, 26 % at 1 °C). After 8 days, comparable biodegradation was observed over a temperature range of 1–15 °C. Biodegradation was negligible at 20 and 25 °C.
The effect of hydrocarbon concentration on biodegradation was examined in the same medium supplemented with 1–20 g diesel oil l-1 and incubated at 15 °C for 4 days, using sterile controls for each concentration tested. Strain A37T could grow in the presence of diesel oil concentrations up to 20 g l-1; approximately 60 % of initial concentrations in the range of 1–10 g l-1 was degraded after 4 days at 15 °C.
The temperature tolerance for protease formation by strain A37T was examined in nutrient broth supplemented with skimmed milk (2 g l-1) at 180 r.p.m. and 1–25 °C. Proteolytic activity was measured by digestion of azocasein, as described by Margesin & Schinner (1992a). Protease production was highest at a cultivation temperature of 15 °C, was approximately 50 % lower at 10 and 20 °C and was negligible at 1 and 25 °C. Strain A37T also hydrolyses gelatin, a property that has been described for only one of six strains of P. africanus and not for P. heparinus, P. piscium or P. saltans (Steyn et al., 1998).
Among cold-adapted micro-organisms, obligate psychrophiles are distinguished from facultative psychrophiles because of differences in ecological distribution and biochemical adaptations (Russell, 1990). Even in permanently cold habitats, such as glacier cryoconite, at least 50 % of the bacteria (Delille & Perret, 1989) or even a greater portion (Herbert, 1986) is not obligately but facultatively psychrophilic, i.e. able to grow from 0 °C to temperatures above 20 °C, with an optimum growth temperature above 15 °C. Strain A37T belongs to this latter group. Like many cold-adapted micro-organisms, strain A37T produces mucous polysaccharide capsules to protect the cells from environmental influences and to retain nutrients (Gounot, 1999). Although the strain was isolated from a non-contaminated environment, a remarkable oil hydrocarbon biodegradation activity was shown. This confirms that cold-adapted oil degraders are ubiquitous (Margesin & Schinner, 2001).
Temperature had a significant effect on hydrocarbon biodegradation, protease production and growth of strain A37T. Despite high cell densities over a temperature range of 10–25 °C, a distinct optimum temperature of 15 °C was noticed for both protease production and oil hydrocarbon biodegradation. The optimum temperature for substrate utilization by cold-adapted micro-organisms is usually significantly below the optimal growth temperature of the producing strains. Thermal inhibition of extracellular enzyme production (Margesin & Schinner, 1992b) and, as demonstrated in this study, of hydrocarbon biodegradation is a common feature of these micro-organisms. The capacity of the isolate described to utilize both natural substrates (protein) and oil hydrocarbons at low temperature points to the ecological significance and biotechnological potential of the microbial community living in cryoconite.
In conclusion, the novel strain, A37T, can be distinguished easily from other Pedobacter species by its facultatively psychrophilic nature, i.e. inability to grow at 28 °C and ability to grow at 1 °C. Another characteristic feature of strain A37T is the ability to degrade oil hydrocarbons, which has not yet been described for other Pedobacter species. Strain A37T can also be distinguished from other Pedobacter species by its ability to assimilate glycogen and 2-ketogluconate.
Description of Pedobacter cryoconitis sp. nov.
Pedobacter cryoconitis (cry.o.co.ni'tis. N.L. gen. n. cryoconitis from cryoconite).
On nutrient agar, colonies are light-yellow, round, convex, mucoid, with entire margins. Cells are rod-shaped (0·7–0·9 µm in diameter and 1·5–3·0 µm long), Gram-negative, non-spore-forming, non-flagellated and motile by gliding. Oxidase, catalase, DNase, amylase, -glucosidase, -galactosidase, protease and -lactamase are positive. Negative for activity of arginine dihydrolase, urease, lipase and tryptophan deaminase, nitrate reduction, H2S production from thiosulfate, indole production and growth on MacConkey agar. Growth occurs between 1 and 25 °C and pH 5–8 in R2A medium, with optimum growth at 20 °C (facultatively psychrophilic) and pH 7. No growth at 28 °C or higher. The optimum temperature for biodegradation of diesel oil and for protease production is 15 °C. The strain assimilates L-arabinose, D-xylose, galactose, D-glucose, D-fructose, D-mannose, methyl -D-glucoside, arbutin, salicin, cellobiose, maltose, lactose, melibiose, sucrose, trehalose, inulin, D-raffinose, starch, glycogen, -gentiobiose, D-turanose, gluconate and 2-ketogluconate. Dominant fatty acids (51 %) are iso-15 : 0 2-OH and 16 : 17c. The G+C content of the DNA of the type strain is 43·4 mol%.
The type strain, A37T (=DSM 14825T=LMG 21415T), was isolated from alpine glacier cryoconite on the Stubaier Glacier in the Tyrolean Alps, Austria.
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S. Shivaji, P. Chaturvedi, G. S. N. Reddy, and K. Suresh Pedobacter himalayensis sp. nov., from the Hamta glacier located in the Himalayan mountain ranges of India Int J Syst Evol Microbiol, May 1, 2005; 55(3): 1083 - 1088. [Abstract] [Full Text] [PDF]
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B. Vanparys, K. Heylen, L. Lebbe, and P. De Vos Pedobacter caeni sp. nov., a novel species isolated from a nitrifying inoculum Int J Syst Evol Microbiol, May 1, 2005; 55(3): 1315 - 1318. [Abstract] [Full Text] [PDF]
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