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1 Department of Biological Sciences, PO Box 8007, Idaho State University, Pocatello, ID 83209, USA
2 Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, PA 16802, USA
Correspondence
Vanya I. Miteva
vim1{at}psu.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain LV3T is AJ459101.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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), and the characterization of their cold-active enzymes. We have isolated numerous psychrophilic micro-organisms and characterized several cold-active 
-galactosidases (Coombs & Brenchley, 1999; de Prada et al., 1996; Gutshall et al., 1995, 1997; Loveland et al., 1994; Loveland-Curtze et al., 1999; Sheridan & Brenchley, 2000). Many of these strains were members of the high-G+C actinomycete–coryneform diverse group of bacteria (Stackebrandt & Woese, 1981). A recent psychrophilic isolate from a lake in the Dry Valley region of Antarctica, designated strain LV3T, had unusual features. Scanning electron micrographs that showed cells with unusual, bulbous protrusions present during all stages of growth were of particular interest. Furthermore, unlike previous isolates, these cells did not have traits typical of members of the genus Arthrobacter, such as a rod–coccus morphological cycle and lysine as the characteristic diamino acid in the peptidoglycan (Loveland-Curtze et al., 1999).
Analyses of the 16S rRNA gene sequence from strain LV3T showed that it was related to, but distinct from, genera such as Agreia, Leifsonia, Subtercola, Agrococcus and Agromyces in the family Microbacteriaceae. This group was recently revised with the addition of novel genera, because analysis of 16S rRNA gene sequences had demonstrated that many of the classical groupings were not monophyletic. The genus Leifsonia was proposed in an attempt to create order within this sub-branch of the actinomycete–coryneform bacterial phylogenetic tree (Evtushenko et al., 2000). For example, the organisms formerly known as Clavibacter xyli subsp. cynodontis and subsp. xyli were reclassified as Leifsonia xyli subsp. cynodontis and Leifsonia xyli subsp. xyli, respectively. At the time of writing, there are five species with validly published names in the genus Leifsonia, which form a distinct phylogenetic branch close to the Agromyces cluster.
We describe here the unusual morphological, chemotaxonomic and phylogenetic characteristics of the psychrophilic strain LV3T. Based on unique features and distinct phylogenetic placement, Rhodoglobus vestalii gen. nov., sp. nov. is proposed for strain LV3T.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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) and incubated at 10 °C until the culture became turbid. Organisms were isolated on instant ocean agar by using streak-plating techniques (Loveland-Curtze et al., 1999) and colonies were passed at least three times to ensure purity. Isolates were streaked onto instant ocean agar with 100 mg X-Gal l-1, to determine those that produced -galactosidase. A red-pigmented colony designated strain LV3T that hydrolysed X-Gal was chosen for further study.
Physiological and biochemical characteristics.
The ability of the strain to grow at different temperatures and on various media was tested by inoculating cells from a turbid culture grown in R2 broth (Difco) onto plates of R2 agar, Luria–Bertani agar, trypticase soy agar without added carbohydrate, nutrient agar, marine agar and instant ocean agar. The cultures were incubated aerobically at -2, 10, 18, 25 and 37 °C. Growth rates were determined by inoculating cells from a turbid culture grown in trypticase soy broth without added carbohydrate (TSB) into fresh TSB to a Klett reading of 10–15, and by incubating aerobically at -2, 5, 10, 18, 21, 22 and 23 °C. API CORYNE test strips (bioMérieux) were used for general characterization of enzymic and fermentation activities and gelatin hydrolysis. The strips were incubated at 18 °C and the results were recorded after 24 and 48 h.
Electron microscopy.
Cells were grown in TSB at 10 or 18 °C for scanning electron microscopy (SEM). They were washed in 0·1 M sodium cacodylate buffer (pH 7·4), filtered onto a 0·2 µm pore polycarbonate filter and fixed in 2·5 % glutaraldehyde in 0·1 M sodium cacodylate buffer for 4 h at 4 °C. After washing, the filters and cells were post-fixed with 1 % OsO4 in 0·1 M sodium cacodylate buffer (pH 7·4) and dried in a BAL-TEC model CPD 030 critical point dryer. The preparations were mounted onto aluminium holders, sputter-coated with 10 nm Au/Pd and observed by SEM (JEOL model 5400) at 30 kV.
For transmission electron microscopy (TEM), cells were pelleted and resuspended in 1–2 % glutaraldehyde in 0·1 M sodium cacodylate buffer (pH 7·4) overnight at 4 °C. After a secondary fixation with 1 % OsO4 in 0·1 M sodium cacodylate buffer (pH 7·4), the cells were dehydrated through an alcohol gradient series, infiltrated with an acetone–Spurrs mixture and polymerized in Spurrs resin. Ultrathin sections were taken, stained with 2 % uranyl acetate in ethanol and lead citrate and observed by TEM (JEOL model 1200 EXII) at 80 kV. Both the SEM and TEM pictures were taken at the Penn State Electron Microscope Facility.
16S rRNA gene amplification and phylogenetic analyses.
Genomic DNA was extracted from strain LV3T using a modification of standard methods (Giovannoni et al., 1990). The 16S rRNA gene was amplified from chromosomal DNA by PCR using Ready-To-Go beads (Amersham Biosciences) and the universal primers 8F and 1492R (Pace et al., 1986; Weisburg et al., 1991). Both strands of the product were sequenced at the Penn State Nucleic Acid Facility on an ABI 370 sequencer. The 16S rRNA gene sequence was aligned with those from the Ribosomal Database Project (RDP) (Maidak et al., 2000) and those obtained from a BLAST search of GenBank (http://www.ncbi.nlm.nih.gov), using the CLUSTAL W program found in the BioEdit platform (version 5.0.6). The alignment was based on 1642 nucleotide positions and was used in maximum-parsimony, maximum-likelihood and distance analyses utilizing the PAUP package (version 4.0b10; Swofford, 2002). The maximum-parsimony method utilized a heuristic search, and both the maximum-likelihood (with a transition–transversion ratio of 2) and distance methods were performed using the neighbour-joining algorithm. The initial distance analysis was performed using the neighbour-joining algorithm and an uncorrected ‘p’ distance in the PAUP program. To determine the effects of using various analysis methods on these results, we compared our results with distance trees generated using the Jukes–Cantor, F81, F84, Kimura two-parameter, Kimura three-parameter, Tamura–Nei, Tajima–Nei and HKY85 models with equal rates for variable sites. Unequal rates for variable sites were also examined for all eight models using 
-parameters with shapes of 0·5, 1·0, 2·0, 3·0, 4·0 and 5·0. Trees generated by all three methods were essentially congruent. A distance matrix was generated from the same alignment by the PAUP program, using the Jukes–Cantor, F81, F84, Kimura two-parameter, Kimura three-parameter, Tamura–Nei, Tajima–Nei and HKY85 models with equal rates for variable sites. The matrices were quite similar. Ten thousand bootstrap replicates were performed for the distance method, using the Jukes–Cantor model with equal rates for variable sites.
Cell-wall analysis.
Cell-wall preparations were hydrolysed and the diamino acids were separated by using a TLC method (Bousfield et al., 1985). Quantitative amino acid analyses were done on cell walls of strain LV3T, prepared according to the short procedure of Schleifer & Kandler (1972), at the University of Michigan Carbohydrate and Structure Facility. For GC-MS analysis, the cell walls were hydrolysed in 6 M HCl at 110 °C and the hydrolysates were dried for 12 h on a Speed Vac Concentrator (Savant Instruments). After derivatization with N-methyl-N-(tert-butyldimethylsilyl)trifluoroacetamide (MTBSTFA; Regis Technologies), the preparations were heated for 1 h at 60 °C. GC-MS cell-wall analysis was carried out at the Penn State Intercollegiate Center for Mass Spectrometry, with a Hewlett Packard model 5972 mass spectrometer.
Fatty acid and lipoquinone analyses.
Fatty acid determinations were done on cells of strain LV3T grown in Luria–Bertani (LB) broth at -2 °C and in TSB at 18 °C. The cells were centrifuged and the pellets frozen at -20 °C and sent to Microbial ID for fatty acid methyl ester analysis. Respiratory lipoquinone analyses were carried out by B. J. Tindall, Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ), Braunschweig, Germany, on freeze-dried cells cultivated in TSB at 18 °C.
DNA base composition.
The G+C content (mol%) was calculated for purified DNA extracted from cells of strain LV3T by determining the melting temperature as described by Mandel & Marmur (1968). The melting temperature of purified chromosomal DNA extracted from Escherichia coli ATCC 23848 was also determined, to serve as an independent control.
Plasmid DNA isolation.
The Wizard Plus SV Minipreps DNA purification kit (Promega) was used for plasmid DNA isolation.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). The upper temperature limit for growth was 22 °C. The cells grew at -2 °C, even though there was an extended lag phase that was independent of the growth temperature of the inoculum. Members of only three other genera in the family Microbacteriaceae (Subtercola, Cryobacterium and Frigoribacterium) have optimal growth temperatures of 18 °C or below. Cryobacterium is the only genus with an upper growth temperature limit lower than that of strain LV3T (Table 1). Formation of reddish intracellular pigment occurred soon after the start of the exponential phase in all cultures. Pigment formation is a common characteristic of representatives of the family Microbacteriaceae (Table 1). The cells also reached a high cell density and remained viable after prolonged incubation in TSB at -2 and 10 °C, with over 1010 c.f.u. ml-1 remaining after 4 months. The cell density dropped to 109 c.f.u. ml-1 after 5 months incubation and there were no viable cells after 7 months.
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). Some of the cells were slightly curved, but lacked the typical fragmented shapes often seen with members of the genus Arthrobacter. The rods were slender and some appeared to enter the 0·2 µm filter pores (Fig. 2a). Most protuberances appeared to be in the central part of the cells. To determine whether the protuberances were formed during a certain growth stage or were due to growth at a specific temperature or in a particular medium, additional cultures that had been grown for different times, at various temperatures and in different media were examined. These structures were observed in pigmented and non-pigmented cells of all growth stages and culture conditions.
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). The micrographs showed uniform cytoplasmic material within the cells, without any disruption of cell-wall integrity or intracellular components in the protuberances. After 150 days incubation, the cells had the same morphology, which showed that the protuberances were not simply cell-wall ‘blebs' being formed in preparation for cell lysis. Although the function of the protuberances is unknown, they appeared to be unrelated to any specific growth stage or condition. It may be that these structures provide an enhanced surface area for nutrient transport for the otherwise small cells, or are the result of an altered rod–coccus cycle, commonly observed among other Gram-positive, non-spore-forming aerobes.
Physiological characteristics
Initially, strain LV3T was chosen for study because it hydrolysed X-Gal, indicating that it might have a cold-active -galactosidase. Other enzymic characteristics were tested using API CORYNE test strips. The strain showed positive enzymic activities for pyrazinamidase, pyrrolidonyl arylamidase, alkaline phosphatase (weak), -galactosidase (weak), 
-glucosidase, -glucosidase and catalase, and was negative for nitrate reductase, -glucuronidase, N-acetyl--glucosidase and urease. It did not hydrolyse gelatin and did not form acid from glucose, ribose, xylose, mannitol, maltose, lactose, sucrose or glycogen. In other tests, the strain did not grow anaerobically or in the presence of 2·5, 5 or 10 % NaCl and did not form heat-resistant spores. A small (approx. 900 bp) plasmid was found in strain LV3T. Further characterization of this plasmid is ongoing.
16S rRNA gene sequence and phylogenetic analysis
The 16S rRNA gene sequence amplified from strain LV3T DNA was analysed using the maximum-parsimony, maximum-likelihood and distance methods. Distance analysis results using the Jukes–Cantor model with equal rates for variable sites are presented (Fig. 3). These results showed that strain LV3T is related to, but phylogenetically distinct from, organisms belonging to the genera Agreia, Subtercola and Leifsonia. The grouping of strain LV3T with the uncharacterized strains ‘Leifsonia rubeus’, Corynebacterium strain QSSC 3-5 and ‘Leifsonia aureus’ was supported by high bootstrap values (Fig. 3).
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). The 16S rDNA sequence of strain LV3T also groups with some less well-characterized strains and is 0·7 % distant from ‘L. rubeus’, 2·12 % from Corynebacterium strain QSSC 3-5 and 2·79 % from ‘L. aureus’. Both ‘L. rubeus’ and ‘L. aureus’ were isolated from a pond in the Wright Valley, Antarctica, which is within 100 miles of the lake from which strain LV3T was isolated. Strains QSSC 3-5 and QSSC 9-20 were isolated from an Antarctic quartz stone sublithic community (Smith et al., 2000) and Cryobacterium psychrophilum JCM 1463T was isolated from Antarctic soil (Suzuki et al., 1997). Although S. boreus K300T, S. frigoramans K265T (Männistö et al., 2000) and Frigoribacterium faeni 801T (Kämpfer et al., 2000) were not isolated from Antarctic samples, they are psychrophilic. Based on the distances between ‘L. rubeus’ and ‘L. aureus’ and the other members of the genus Leifsonia, as well as the distance between strain QSSC 3-5 and the other members of the genus Corynebacterium, these organisms may need to be included in the newly proposed genus Rhodoglobus.
In addition, during analysis of the 16S rRNA gene sequences, we observed that the sequence for strain LV3T contained a 13 bp insertion that was present in only a few related 16S rRNA genes. Insertions with an almost-identical sequence were found in ‘L. rubeus’ and ‘L. aureus’, and insertions with similar sequences were found in S. frigoramans K265T, C. psychrophilum JCM 1463T and strains QSSC 9-20 and WCHB 1-18 (Dojka et al., 1998). However, insertions were not found in S. boreus K300T, S. pratensis DSM 14246T, Agreia bicolorata VKM Ac-1804T (Evtushenko et al., 2001), strain QSSC 3-5 or any of the type strains in the genus Leifsonia. The presence of insertions did not correspond to the isolates' geographical origin or to their mode of growth (psychrophilic). The insertion sequence of strain LV3T was mapped (Fig. 4a) onto the secondary structure of the most closely related organism (Arthrobacter globiformis DSM 20124T) for which a structure has been generated (Gutell, 1994; http://www.rna.icmb.utexas.edu). The partial secondary structure presented in Fig. 4a corresponded to nucleotides 436–476 of the 16S rRNA gene sequence of Arthrobacter globiformis DSM 20124T. As the inserted nucleotides can form a number of possible hairpin structures that would stabilize the insertion (Fig. 4b), it is unlikely that they were artefacts. The combination of the distance of the 16S rRNA gene sequence for strain LV3T from that of other type strains, plus its insertion sequence, supports the designation of strain LV3T as a representative of a novel genus.
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). Most species closely related to strain LV3T also contain significant amounts of branched-chain fatty acids (Table 2). When strain LV3T was cultured at -2 °C, the amount of anteiso-C15 : 0 decreased by 1·5-fold and the amount of the unsaturated fatty acid anteiso-C15 : 1 increased 10-fold. These results are consistent with changes in the ratio of unsaturated and saturated fatty acids found in other Gram-positive non-spore-forming rods grown at different temperatures. For example, Cryobacterium psychrophilum (previously known as ‘Curtobacterium psychrophilum’), which does not grow at above 18 °C, exhibits a decrease in anteiso-C15 : 0 and anteiso-C17 : 0 and a sixfold increase in anteiso-C15 : 1 when cultured at 4 °C (Suzuki et al., 1997). Anteiso-C15 : 1 was found in cells of S. frigoramans when grown at temperatures 
15 °C (Männistö et al., 2000). Adjustment of the fatty acid composition may increase membrane fluidity at lower temperatures. The majority of bacterial species contain straight-chain saturated and unsaturated fatty acids, and maintaining membrane fluidity may be accomplished by increasing the amount of unsaturated and short-chain fatty acids at lower temperatures (Kaneda, 1991).
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). Significant amounts of alanine, glycine and glutamic acid were also found, and only small amounts of lysine were detected. GC-MS results confirmed that lysine was present only in small quantities and homoserine was present only in trace amounts. Based on the results of the quantitative amino acid analyses, the molar ratio of glutamic acid to glycine to alanine to ornithine was 1 : 1·5 : 1·1 : 1·4. Strain LV3T peptidoglycan seems to be closest to type B2 (Schleifer & Kandler, 1972), although the relative amounts of the amino acids are not totally consistent with this type.
Species closely related to strain LV3T have cell walls comprised of type-B peptidoglycan, although the diamino acid differs between the genera of the family Microbacteriaceae. The closest characterized phylogenetic relatives of strain LV3T, including S. boreus and S. frigoramans (Männistö et al., 2000), contain diaminobutyric acid (DAB) as the diamino acid. Agreia bicolorata (Evtushenko et al., 2001) contains both DAB and ornithine; another organism that contains this unusual combination is S. pratensis (Behrendt et al., 2002), which is currently being reclassified. Many Microbacterium species, including reclassified Aureobacterium species (Takeuchi & Hatano, 1998) and Curtobacterium species (Komataga & Suzuki, 1986), contain ornithine. Microbacterium species, Mycetocola saprophilus, Mycetocola tolaasinivorans, Mycetocola lacteus (Tsukamoto et al., 2001) and Okibacterium fritillariae (Evtushenko et al., 2002) contain lysine.
Cells of strain LV3T contained 65 % MK-12, 35 % MK-11 and small amounts of MK-10 and MK-13. The presence of saturated menaquinones is characteristic of members of the family Microbacteriaceae, but close relatives of strain LV3T do not have the same menaquinone composition. For example, MK-10 is the major menaquinone in Agreia bicolorata (Evtushenko et al., 2001) and MK-10 and MK-11 are the major menaquinones in S. pratensis (Behrendt et al., 2002). S. boreus and S. frigoramans (Männistö et al., 2000) have predominantly MK-9 and MK-10. The menaquinone composition of strain LV3T also distinguishes it from other genera in the family Microbacteriaceae.
DNA G+C content
The G+C content for the genomic DNA of strain LV3T was calculated to be 62 mol%, based on its melting temperature. This value is consistent with the G+C content for the 900 bp plasmid found in strain LV3T, which was found to be 59 mol% (V. I. Miteva & J. E. Brenchley, unpublished data). The DNA G+C content for strain LV3T may be another distinguishing feature, as it was slightly lower than those reported for related organisms such as L. poae at 66–73 mol% (Evtushenko et al., 2000) and Agreia bicolorata at 67 mol% (Evtushenko et al., 2001).
Description of Rhodoglobus gen. nov.
Rhodoglobus (Rho.do.glo'bus. Gr. n. rhodon the rose; L. masc. n. globus ball; N.L. masc. n. rhodoglobus red ball).
Cells are aerobic, Gram-positive, easily decolourized, motile and non-spore-forming. Colonies are smooth, round, convex, non-slimy, translucent, reddish and small (2–3 mm in diameter). Individual cells are slender rods (mean cell size of 0·15–0·2x1–1·2 µm), with bulbous protuberances (mean diameter 0·8 µm) seen at all stages of growth. Cells grow aerobically at -2–21 °C. Cell walls contain ornithine as the diagnostic amino acid. Predominant fatty acids are anteiso-C15 : 0, anteiso-C17 : 0 and iso-C16 : 0. Major menaquinones are MK-11 and MK-12. The type species is Rhodoglobus vestalii.
Description of Rhodoglobus vestalii sp. nov.
Rhodoglobus vestalii [ves.ta'li.i. N.L. gen. n. vestalii in honour of the late J. Robie Vestal, who studied Antarctic micro-organisms and was a mentor to one of the authors (P. P. S.)].
The following characteristics are shown in addition to those that define the genus. Cells do not exhibit a marked rod–coccus cycle and grow optimally at 18 °C. G+C content of the DNA is approximately 62 mol%. Major cellular fatty acids are anteiso- and iso-branched fatty acids. When cells are grown at -2 °C, the amount of the unsaturated fatty acid anteiso-C15 : 1 increases substantially and the amount of anteiso-C15 : 0 decreases. Cells show positive enzymic activities for pyrazinamidase, pyrrolidonyl arylamidase, alkaline phosphatase (weak), -galactosidase (weak), -glucosidase, -glucosidase and catalase, but are negative for nitrate reductase, -glucuronidase, N-acetyl--glucosidase and urease. Cells do not hydrolyse gelatin and do not form acid from glucose, ribose, xylose, mannitol, maltose, lactose, sucrose or glycogen. The 16S rRNA gene sequence contains an insertion of 13 nucleotides that is shared with some of its most closely related neighbours.
The type strain, LV3T (=ATCC BAA-534T =CIP 107482T), was isolated from an Antarctic Dry Valley lake.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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