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1 Institut für Mikrobiologie, Universität Innsbruck, Technikerstraße 25, A-6020 Innsbruck, Austria
2 DSMZ – Deutsche Sammlung für Mikroorganismen und Zellkulturen GmbH, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
3 Laboratory of Microbial Ecology, UMR 5557, University Claude Bernard Lyon 1, F-69622 Villeurbanne-Cedex, France
Correspondence
Rosa Margesin
rosa.margesin{at}uibk.ac.at
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ABSTRACT |
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L-lys–L-Glu-type peptidoglycan and contained glucose as the only cell-wall sugar. MK-10 was the predominant menaquinone, and the polar lipid pattern consisted of phosphatidylglycerol, diphosphatidylglycerol, phosphatidylinositol and an unidentified glycolipid. Strain AG31T (=DSM 15454T=LMG 21914T) is assigned as the type strain of a novel Arthrobacter species, Arthrobacter psychrophenolicus sp. nov.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain AG31T is AJ616763.
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TOPABSTRACTMAIN TEXTREFERENCES |
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; Margesin & Schinner, 1999; Margesin et al., 2002). A wide diversity of cold-adapted micro-organisms can be found in various cold environments. A particular cold environment is found in caves situated in cold areas. Caves in mountain areas have a constant low temperature near 0 °C and lack freeze–thaw cycles; this is favourable to the selection of cold-adapted bacteria (Gounot, 1999). Bacteria with coryneform morphology, such as Arthrobacter, are widespread among bacteria found in caves (Khizhnyak et al., 2003). Psychrophilic Arthrobacter strains were reported to be the most abundant and active bacteria in subterranean cave silts (Gounot, 1967) and were also isolated from glacier silts (Moiroud & Gounot, 1969), Arctic soils (Juck et al., 2000) and Antarctic environments (Loveland-Curtze et al., 1999; Reddy et al., 2000, 2002; Stibor et al., 2003). Representatives of cold-adapted Arthrobacter strains produce cold-active enzymes with interesting properties (Nakagawa et al., 2003; Stibor et al., 2003). However, there is little information on Arthrobacter strains able to degrade hydrocarbons at low temperatures, although high-G+C coryneform bacteria are considered important members of hydrocarbon-degrading microbial populations (Bej et al., 2000; Juck et al., 2000; Margesin et al., 2003a). A cold-adapted representative of the genus Arthrobacter isolated from an alpine ice cave has been described recently as degrading high phenol concentrations at low temperatures (Margesin et al., 2003b). This strain was subjected to phenotypic, chemotaxonomic, genetic and phylogenetic examinations. Strain AG31T was isolated from a carbonate-rich deposit collected under sterile conditions in the autumn of 1999 in an alpine ice cave (Eisriesenwelt Werfen) located in Salzburg, Austria, at about 1640 m above sea level. A 10 g sample was shaken with 90 ml sterile 1 % (w/v) sodium pyrophosphate for 20 min at 350 r.p.m. Appropriate dilutions, prepared with sterile distilled water, were plated (0·1 ml) on soil-extract agar incubated at 4 °C. The medium contained 50 % (v/v) soil extract (pH 7), 0·05 % (w/v) yeast extract, 0·05 % (w/v) peptone from soymeal and 1·2 % (w/v) agar (pH 7).
Genomic DNA extraction and PCR-mediated amplification of the 16S rRNA gene were done as described previously (Rainey et al., 1996). PCR products were sequenced according to the manufacturer's instructions using a CEQ DCTS quick start kit (Beckman Coulter) and a CEQ8000 automatic sequencing system (Beckman Coulter). The 16S rRNA gene sequence was aligned manually with published sequences from representatives of the Actinobacteria contained in the database of 16S rRNA gene sequences held by the DSMZ. The ae2 editor (Maidak et al., 1999) was used to align the 16S rRNA gene sequence of strain AG31T against the sequences of the Arthrobacter 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 phylogenetic analysis included all reported species of the genus Arthrobacter. The analysis based on the almost complete 16S rRNA gene sequence (1501 nt) of strain AG31T indicated that Arthrobacter sulfureus DSM 20167T was the closest phylogenetic neighbour, displaying 98·3 % sequence similarity to strain AG31T (Fig. 1).
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. DNA–DNA hybridization was carried out as described by De Ley et al. (1970), with the modifications described by Huß et al. (1983) and Escara & Hutton (1980), using a model 2600 spectrophotometer equipped with a model 2527-R thermoprogrammer and plotter (Gilford Instrument Laboratories). Renaturation rates were computed with the TRANSFER.BAS program of Jahnke (1992). DNA from strain AG31T showed only 29·9 % DNA–DNA relatedness to A. sulfureus.
Analysis of fatty acid methyl esters was performed by GLC as described by Miller (1982) and Sasser (1990). The cellular fatty acids of strain AG31T grown at 25 °C were identified as anteiso-C15 : 0 (72·1 %), anteiso-C17 : 0 (7·0 %), iso-C16 : 0 (8·3 %), iso-C15 : 0 (5·6 %), C16 : 0 (2·8 %), iso-C14 : 0 (2·1 %), anteiso-C13 : 0 (0·9 %), iso-C17 : 0 (0·7 %) and C14 : 0 (0·7 %). The presence of significant amounts of the predominant fatty acid anteiso-C15 : 0 is characteristic of representatives of the genus Arthrobacter (Keddie et al., 1986); anteiso 12-methyl tetradecanoic acid is also the predominant fatty acid in A. sulfureus (Stackebrandt et al., 1983).
The peptidoglycan structure, menaquinones and polar lipids were determined as described by Groth et al. (1997) and cell-wall sugars were analysed according to Staneck & Roberts (1974). Analysis of the peptidoglycan structure of strain AG31T revealed it to be of the A4 type (Schleifer & Kandler, 1972) with an interpeptide bridge consisting of L-Glu, type A11.54, according to the DSMZ (2001). To date, this peptidoglycan type has been reported within the genus Arthrobacter only for A. sulfureus (Schleifer & Kandler, 1972). Strain AG31T contains menaquinones MK-10, MK-9 and MK-11 (ratio of peak areas, 72 : 12 : 1, respectively). A. sulfureus, the closest neighbour phylogenetically, differs from strain AG31T in displaying MK-9 as the predominant component and possessing MK-10, MK-8 and MK-7 only in small amounts (Yamada et al., 1976). Arthrobacter nicotianae is phylogenetically related to strain AG31T but differs in its peptidoglycan structure and menaquinone composition (Table 1). The polar lipid pattern of strain AG31T consists of phosphatidylglycerol, diphosphatidylglycerol, phosphatidylinositol and an unidentified glycolipid. Glucose was detected as the only cell-wall sugar (Table 1).
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; Stackebrandt & Schumann, 2000), A. nicotianae DSM 20123T, as an established representative of this group of highly related Arthrobacter species, was also chosen for comparison. Morphology and motility were examined by using phase-contrast microscopy (1000x) of cells grown on nutrient agar (pH 7) plates at 25 °C over 48 h. Testing for the Gram reaction was carried out using classical Gram-staining and was confirmed by the KOH-lysis test and the aminopeptidase activity test (Bactident; Merck) as described by Süßmuth et al. (1987). Sensitivity to antibiotics was determined with ATB strips (bioMérieux) incubated for up to 48 h at 25 °C. The biochemical profile was determined with API CORYNE and API 20NE strips (bioMérieux) incubated at 25 °C for up to 48 h; the profile of strain AG31T was also determined at 10 °C. The ability to utilize glucose was additionally tested by growing the strains in a pH-neutral minimal medium with glucose (0·2 %, w/v) as the sole carbon source. Thiosulfate formation, motility and indole formation were tested by using SIM agar (Süßmuth et al., 1987). The presence of enzyme activities was determined with API ZYM strips incubated at 30 °C for 6 h. Additionally, amylase, protease, pectolytic enzymes, 
-galactosidase, lipase and -lactamase activities were tested on nutrient agar (pH 7) plates supplemented with starch, skimmed milk, polygalacturonic acid (each at 0·4 %, w/v), lactose and X-Gal (0·2 %, w/v, and 0·004 %, w/v, respectively) or ampicillin (50 µg ml–1) as described by Margesin et al. (2003b) and incubated at 10 and 25 °C.
The properties of strain AG31T are indicated in the species description; the diagnostic characteristics that differentiate the strain from A. sulfureus and A. nicotianae are shown in Table 1
. Colonies of strain AG31T displayed a yellow, non-fluorescent pigment on nutrient agar; this pigment was lost when the strain was grown on minimal medium agar plates with phenol as the sole carbon source. In comparison, Arthrobacter chlorophenolicus produced its pearl-grey pigment in the presence of a number of phenolic compounds only under growth conditions involving low oxygen availability (Westerberg et al., 2000). A number of species of the genus Arthrobacter, such as Arthrobacter aurescens, Arthrobacter citreus, Arthrobacter ilicis, A. nicotianae, Arthrobacter protophormiae, A. sulfureus, Arthrobacter uratoxydans, Arthrobacter mysorens (Stackebrandt et al., 1983; Keddie et al., 1986) and Arthrobacter flavus (Reddy et al., 2000) were described as producing a yellow pigment. On the other hand, fewer than 1 % of 515 Arthrobacter strains isolated from caves were pigmented (Gounot, 1999). This might be an indication that strain AG31T does not belong to the indigenous cave population but was probably introduced from outside, since caves visited by tourists contain a large number of introduced micro-organisms.
To determine the pH tolerance for growth, the strains were cultivated aerobically at 180 r.p.m. in 100 ml Erlenmeyer flasks containing 10 ml nutrient broth (pH 5–11). Growth at 10 and 25 °C was monitored over 24–72 h by measuring the optical density at 600 nm. The pH range for growth of strain AG31T was 6–10, with optimum growth at pH 8–10 (corresponding to the alkaline conditions of the natural habitat). Growth of A. sulfureus and A. nicotianae was optimal at pH 7–9 and 7–8, respectively. None of the strains could grow at pH 5 or 11.
Salt tolerance was determined by monitoring growth in nutrient broth supplemented with 1–10 % (w/v) NaCl. The presence of 1–3 % (w/v) NaCl was not growth-inhibiting but actually growth-stimulating, while concentrations of 5 or 10 % (w/v) NaCl inhibited growth significantly or completely, respectively.
The effect of temperature (1–37 °C) on growth was examined in complex medium (nutrient broth) and in minimal medium composed of 0·35 % Na2HPO4.2H2O, 0·2 % KH2PO4, 0·1 % (NH4)2SO4, 0·005 % Ca(NO3)2.4H2O, 0·001 % ammonium iron(III) citrate and 0·02 % MgSO4.7H2O (pH 7) and containing 5 mM phenol as the sole carbon source. Growth was tested both in liquid culture and on agar plates. Strain AG31T exhibited the properties of a facultative psychrophile (Morita, 1975), showing good growth at temperatures ranging from 1 to 25 °C. No growth occurred at 37 °C. After 24 h cultivation in complex medium, growth was optimal at 25 °C. After 48 and 72 h, however, comparable cell densities were obtained at 15–25 °C and 10–25 °C, respectively. The highest cell density was obtained at 1 °C, while A. sulfureus and A. nicotianae produced the largest amount of biomass at 25 °C and 20–30 °C, respectively. These data demonstrate the cold-adapted character of strain AG31T. Slow growth at 30 °C was observed only after 4 days cultivation in liquid nutrient broth culture but was not observed in nutrient agar or in liquid or solid minimal medium with phenol.
None of the strains tested could utilize diesel oil (1000 mg l–1) or n-hexadecane (700 mg l–1) for growth, whereas both strain AG31T and A. sulfureus degraded phenol. Strain AG31T fully degraded 5 mM phenol within 2 days cultivation at 15–25 °C; full degradation had also occurred after 3 days at 10 °C and after 7 days at 1 °C. In comparison, A. sulfureus degraded phenol at temperatures below 20 °C slower than did strain AG31T.
Phenol degradation by strain AG31T was further investigated using fed-batch cultivation in minimal medium containing phenol as the sole carbon source, whereby the same culture was recontaminated with increasing (1–12·5 mM) phenol concentrations as soon as the phenol from the previous addition had disappeared (Margesin et al., 2003a). The strain degraded up to 7·5 mM phenol within 3 days at 10 °C, while 10 mM phenol was utilized within 7 days; 12·5 mM phenol had a toxic effect. A. sulfureus even degraded 15 mM phenol at 25 °C, which may be attributable to the natural habitat (oil brine) of the strain. Since there was no abiotic loss of phenol in sterile controls, phenol disappearance was due to biodegradation. Strain AG31T (Margesin et al., 2003b, 2004) and A. sulfureus produced a significantly higher amount of catechol-1,2-dioxygenase than of catechol-2,3-dioxygenase, indicating the preferred oxidation of catechol by the ortho type of ring cleavage.
The new strain, AG31T, can be easily distinguished from A. sulfureus DSM 20167T, the strain with the closest phylogenetic relationship, by its inability to grow at 30 °C and to assimilate glucose. Inability to assimilate glucose is rarely found with Arthrobacter strains, since more than 90 % of tested strains utilized this carbon source (Keddie et al., 1986). Other characteristic properties are indicated in Table 1. Additionally, the combination of chemotaxonomic characteristics (peptidoglycan type A4 with an interpeptide bridge consisting of L-Glu; MK-10 as the predominant menaquinone) serve to distinguish the novel bacterium from all recognized Arthrobacter species. Therefore, on the basis of phenotypic, phylogenetic and chemotaxonomic evidence, we propose that the bacterial strain should be classified within the genus Arthrobacter, as the type strain of Arthrobacter psychrophenolicus sp. nov.
Description of Arthrobacter psychrophenolicus sp. nov.
Arthrobacter psychrophenolicus (psy.chro.phe.no'li.cus. Gr. adj. psychros relating to cold; N.L. masc. adj. phenolicus relating to phenol degradation; N.L. masc. adj. psychrophenolicus relating to phenol degradation at low temperatures).
On nutrient agar, colonies are round, convex, glossy, with entire margins and have a yellow, non-fluorescent pigment. Cells are Gram-positive, aerobic, non-spore-forming, non-motile and exhibit a rod–coccus cycle with irregular rods in the exponential growth phase and predominantly coccoid cells in the stationary growth phase. Physiological and biochemical properties are indicated in Table 1. Good growth and phenol biodegradation occur between 1 and 25 °C (facultative psychrophile). Fully degrades up to 10 mM phenol as the sole carbon source. No growth occurs at pH 5 or 11. The predominant fatty acid (72·1 %) is anteiso-C15 : 0. The peptidoglycan type is A4 L-lys–L-Glu. MK-10 is the predominant menaquinone, while MK-9 and MK-11 occur in smaller amounts. The polar lipids are phosphatidylglycerol, diphosphatidylglycerol, phosphatidylinositol and an unidentified glycolipid.
The type strain is AG31T (=DSM 15454T=LMG 21914T), isolated from an alpine ice cave in Werfen (Salzburg), Austria.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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