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Laboratorium voor Microbiologie, Vakgroep Biochemie, Fysiologie en Microbiologie, Universiteit Gent, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium
Correspondence
Stefanie Van Trappen
stefanie.vantrappen{at}UGent.be
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ABSTRACT |
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-subclass of the Proteobacteria. Sequence similarity values for the strains with their nearest phylogenetic neighbours (Jannaschia, Octadecabacter and Ketogulonicigenium) ranged between 94·0 and 95·8 %. DNA–DNA hybridizations and comparison of repetitive extragenic palindromic DNA–PCR (rep-PCR) fingerprinting patterns revealed that these strains are members of three distinct species. The isolates are Gram-negative, chemoheterotrophic, non-motile rods and their DNA G+C contents range from 59·4 to 66·4 mol%. Whole-cell fatty acid profiles are similar and the primary fatty acid in all the strains is 18 : 1 
7c (74·1–87·7 % of total). Genotypic results together with phenotypic characteristics allowed the differentiation of these species from related recognized species of the -Proteobacteria and the strains are assigned to a new genus, Loktanella gen. nov., with three novel species: Loktanella salsilacus sp. nov. (type species), consisting of ten strains with LMG 21507T (=CIP 108322T) as type strain; Loktanella fryxellensis sp. nov., consisting of 12 strains with LMG 22007T (=CIP 108323T) as type strain; and Loktanella vestfoldensis sp. nov., consisting of four strains with LMG 22003T (=CIP 108321T) as type strain.
Published online ahead of print on 23 January 2004 as DOI 10.1099/ijs.0.3006-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains LMG 22007T, LMG 22003T, LMG 21507T, LMG 22000, LMG 22002 and LMG 22006 are AJ582225, AJ582226, AJ440997, AJ582228, AJ582229 and AJ582227, respectively.
Normalized rep-PCR profiles and a dendrogram are available as supplementary material in IJSEM Online.
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-subclass of the Proteobacteria, in which they are phylogenetically related to the genus Rhodobacter. The abundance of some members from the Rhodobacter group in these aquatic environments has been correlated with the presence of algal blooms and it has been suggested that they play an important role in sulfur cycling (González et al., 1999
, 2000).
Several of these novel members originate from Antarctic habitats: Antarctobacter heliothermus (Labrenz et al., 1998), Roseovarius tolerans (Labrenz et al., 1999), Staleya guttiformis and Sulfitobacter brevis (Labrenz et al., 2000) from Ekho Lake, and Octadecabacter arcticus and Octadecabacter antarcticus (Gosink et al., 1997) from polar sea ice and sea water. Recently, two new genera have been added to this Rhodobacter group: Ketogulonicigenium (Urbance et al., 2001), isolated from soil and which oxidizes L-sorbose to 2-keto-L-gulonic acid, and Jannaschia helgolandensis (Wagner-Döbler et al., 2003), isolated from the North Sea.
During the MICROMAT project (November 1998 to February 2001), 746 heterotrophic bacterial strains were isolated from microbial mat samples, collected from ten Antarctic lakes (Van Trappen et al., 2002). Numerical analysis of the fatty acid composition of the isolates revealed 41 clusters, and 16S rRNA gene sequence analysis, performed on representative strains, showed that they belong to the -, 
- and 
-subclasses of the Proteobacteria, the Gram-positives and the Bacteroidetes (Van Trappen et al., 2002). Fatty acid analysis and 16S rRNA gene sequence analysis showed that diversity of heterotrophic bacteria in microbial mats from Antarctic lakes is very high. Moreover, many fatty acid clusters were shown to contain multiple taxa when tested by repetitive extragenic palindromic DNA–PCR (rep-PCR) fingerprinting, a technique used to investigate the genomic diversity of each fatty acid cluster in greater detail, especially those belonging to the Bacteroidetes group (Van Trappen et al., 2003, 2004).
In the present work we studied the relationships of 26 strains from fatty acid cluster 41 (Van Trappen et al., 2002, belonging to the -Proteobacteria), using polyphasic taxonomic characterization.
The investigated isolates, their origin and genomic profile grouping are given in Table 1. Strains were routinely cultivated on marine agar 2216 (Difco) at 25 °C for 48 h, except when indicated otherwise.
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. rep-PCR fingerprinting (based on primers targeting the repetitive extragenic palindromic sequence) was performed on all strains of fatty acid cluster 41 (59 strains) isolated by Van Trappen et al. (2002), using the primers GTG5 and REP1R-I and REP2-I (Versalovic et al., 1991), as described by Rademaker & de Bruijn (1997) and Rademaker et al. (2000). Numerical analysis was carried out using the BIONUMERICS software package (Applied Maths). Twenty-six of these strains, listed in Table 1
, could be divided into three different clusters according to their combined profile type (available as supplementary material in IJSEM Online) and these clusters were delineated by numerical analysis at a Pearson correlation coefficient level of 50 %. They are hereafter referred to as rep-PCR profile type I (comprising 12 strains), type II (four strains) and type III (ten strains). It is now well established that similar rep-PCR profiles are correlated to high total genomic DNA–DNA hybridization values (Versalovic et al., 1994; Rademaker & De Bruijn, 1997; Rademaker et al., 2000; Van Trappen et al., 2003, 2004).
The almost-complete 16S rRNA gene sequences (1404–1449 nt) of strains LMG 22003T, LMG 22006, LMG 22007T, LMG 21507T, LMG 22000 and LMG 22002 were determined as described previously (Van Trappen et al., 2004). The closest related sequences were found using the FASTA program and the sequences from reference strains were aligned, with editing of the alignment and reformatting performed with the BIOEDIT program (Hall, 1999) and FORCON (Raes & Van de Peer, 1999). Evolutionary distances were calculated using the evolutionary model of Jukes and Cantor and a phylogenetic tree (shown in Fig. 1) was constructed using the neighbour-joining method (Saitou & Nei, 1987) with the TREECON program (Van de Peer & De Wachter, 1994). Dendrograms obtained by maximum-parsimony and maximum-likelihood analyses showed essentially the same topography (data not shown).
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-Proteobacteria and are associated with the Rhodobacter group. A phylogenetic tree showing the position of the strains to their closest neighbours is shown in Fig. 1.
The 16S rRNA gene sequence of strain LMG 22007T (representative for the strains of rep-PCR profile type I) revealed 98·6 % similarity to that of strain LMG 21507T (identical to that of LMG 22000 and LMG 22002, and representative for rep-PCR profile type III) and 95·4 % to that of strain LMG 22003T (identical to that of strain LMG 22006, and representative for rep-PCR profile type II). The strains with nearest related sequences to that of strain LMG 22007T (rep-PCR profile I) were J. helgolandensis Hel 10T (95·8 %), O. antarcticus 307T (94·5 %) and the currently unclassified marine alpha proteobacterium strain QSSC9-5 (97·3 %). The 16S rRNA gene sequence of strain LMG 22003T (rep-PCR profile type II) showed 95·4 % sequence similarity to J. helgolandensis Hel 10T, 94·2 % to Ketogulonicigenium vulgare DSM 4025T, 94·3 % to Ruegeria algicola DSM 10251T and 96·2 % to the currently unclassified strain AS-26. The 16S rRNA gene sequence of strain LMG 21507T (rep-PCR profile type III) showed 95·7 % similarity to J. helgolandensis Hel 10T, 94·2 % to O. antarcticus 307T, 94·2 % to K. vulgare DSM 4025T and 98·4 % to strain QSSC9. The low level of sequence similarities of the novel strains with recognized bacteria belonging to the Rhodobacter group of the -Proteobacteria (91·0–95·8 %) clearly demonstrates that they represent a new genus.
Genomic relatedness between the novel Antarctic strains, representing the three different rep-PCR profile types, was determined by DNA–DNA hybridizations. DNA was prepared according to the method of Marmur (1961) and DNA–DNA hybridizations were carried out with photobiotin-labelled probes in microplate wells as described by Ezaki et al. (1989), using an HTS7000 Bio Assay Reader (Perkin Elmer) for fluorescence measurements. Hybridization temperature was 45 °C and reciprocal experiments were performed for every pair of strains. The mean hybridization level between strains LMG 22007T (rep-PCR profile type I), LMG 22003T (rep-PCR profile type II) and LMG 21507T (rep-PCR profile type III) ranged between 10·5 and 17·6 %, indicating that the strains represent three different species (Wayne et al., 1987). Differences between reciprocal experiments were less than 10 %. The rep-PCR profiles within each of the clusters I and II were almost identical (see Table 1 and supplementary data in IJSEM Online), indicating that within each of these clusters strains represent a single species (Versalovic et al., 1994). Indeed, the 16S rRNA gene sequences of two strains from rep-PCR group II are identical. Hybridization values of the three representative strains (LMG 21507T, LMG 22000 and LMG 22002) of rep-PCR profile type III were between 78·2 and 85·5 %, indicating that these strains represent a single new species, as would be expected from their identical 16S rRNA gene sequences.
The G+C content of the DNA from the Antarctic strains was determined using an HPLC method, as described by Van Trappen et al. (2003). G+C values of strains LMG 22007T, LMG 22008, LMG 22009 and LMG 22010 from rep-PCR cluster I are 65·7, 66·2, 66·4 and 66·3 mol%, respectively; values for strains LMG 22003T, LMG 22004, LMG 22005 and LMG 22006 from rep-PCR cluster II are 62·1, 62·6, 62·3 and 63·1 mol%, respectively; and values for strains LMG 21507T, LMG 21999, LMG 22000, LMG 22001 and LMG 22002 of rep-PCR cluster III are 60·4, 60·3, 59·7, 60·1 and 59·4 mol%, respectively. These values are consistent with the G+C content of the Rhodobacter group, which ranges between 52·1 and 65 mol% (Labrenz et al., 2000; Urbance et al., 2001; Wagner-Döbler et al., 2003; González et al., 2003).
Cellular fatty acid patterns of the Antarctic strains are based on the data generated by Van Trappen et al. (2002). The strains showed similar fatty acid profiles (see Table 2), with the most abundant fatty acid being 18 : 1 7c, accounting for 74·1–87·7 % of the total fatty acids. This profile is characteristic for several major phylogenetic groups of the -Proteobacteria. Other fatty acids, in lower proportions, are 10 : 0 3OH, 16 : 0, 18 : 0 and summed feature 7 (comprising the unknown fatty acid 18.846, 19 : 1 6c and 19 : 0 cyclo 10c). The Antarctic strains can be differentiated from phylogenetic neighbour J. helgolandensis by the relative amount of 18 : 1 7c (45–52 %) and 19 : 0 cyclo (20–25 %) and from Ketogulonicigenium species by the relative amount of 16 : 0 (32–39 %) and 18 : 1 7c (41–55 %). The strains belonging to the different rep-PCR clusters can be differentiated from each other by the presence or absence of, for example, summed feature 2 (comprising any combination of 12 : 0 aldehyde, unknown 10.928, 16 : 1 iso I and 14 : 0 3OH), 18 : 1 7c 11 methyl and the unknown fatty acid 11.799.
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Colony morphology was determined on marine agar after 7 days. In addition, growth and adherence of colonies on R2A, nutrient and trypticase/soy agars were tested. Cells were tested for their reaction to the Gram stain and for catalase and oxidase activity. Tests in the commercial systems API ZYM, API 20NE and API 20E (bioMérieux) were generally performed according to the manufacturer's instructions. The API ZYM tests were read after 4 h incubation at 25 °C, the other API tests after 48 h at 25 °C. Degradation of casein (Reichenbach & Dworkin, 1981), DNA (using DNA agar from Difco, supplemented with 0·01 % toluidine blue from Merck), starch, Tween 80 and L-tyrosine (Barrow & Feltham, 1993) was tested and reactions were read after 5 days.
The strains show the typical morphological characteristics of the Rhodobacter group (Labrenz et al., 2000; Urbance et al., 2001; Wagner-Döbler et al., 2003; González et al., 2003) and their physiological and biochemical characteristics are given in the descriptions below. The strains of rep-PCR clusters I, II and III can be differentiated from each other and related genera by several phenotypic characteristics (see Table 3 and Table 4).
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Description of Loktanella gen. nov.
Loktanella (Lok.tan.el'la. N.L. fem. n. Loktanella named after Tjhing-Lok Tan from the Alfred Wegener Institute in Bremerhaven, who contributed to our understanding of marine and polar bacteriology and ecology).
Gram-negative, rod-shaped cells that are strictly aerobic, moderately halotolerant and chemoheterotrophic. They do not form spores and the optimal growth temperature is 25 °C. Motility is not observed. Cytochrome oxidase-, catalase- and -galactosidase-positive. The dominant fatty acid is 18 : 1 7c and other characteristic fatty acids are 10 : 0 3OH, 16 : 0, 18 : 0 and summed feature 7 (which comprises the unknown fatty acid 18.846, 19 : 1 6c and 19 : 0 cyclo 10c). The DNA G+C content ranges from 59·4 to 66·4 mol%. As determined by 16S rRNA gene sequence analysis, the genus Loktanella belongs to the Rhodobacter group within the -Proteobacteria.
The type species is Loktanella salsilacus.
Description of Loktanella salsilacus sp. nov.
Loktanella salsilacus (sal.si.la'cus. L. adj. salsus salt, salty; L. gen. n. lacus of a lake; N.L. gen. n. salsilacus of a salt lake, referring to the isolation source, Ace Lake and Organic Lake, Vestfold Hills, Antarctica).
Cells are Gram-negative, short rods (<1 µm by 3–4 µm), often forming pairs or short chains. Strains grow at 5–30 °C; weak growth is observed at 37 °C and no growth occurs at 45 °C. Beige, convex, translucent colonies with a diameter of 1–2 mm, with entire margins are formed on marine agar plates. Growth also occurs on R2A, but no growth is observed on trypticase/soy agar and nutrient agar. Colonies do not adhere to the agar. Degrades aesculin, Tween 80 and citrate. Growth on carbohydrates (API 20NE) is not observed and acids from carbohydrates are not produced (API 20E). Agar, casein, DNA, gelatin, starch, tyrosine and urea are not degraded. Tests for indole production, nitrate reduction, the Voges–Proskauer reaction and hydrogen sulfide production are negative. None of the strains shows activity for the enzymes arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase (API 20E) and lipase (C14), valine arylamidase, cystine arylamidase, -chymotrypsin, trypsin, -galactosidase, -glucuronidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase (API ZYM). Weak enzymic activity is observed for alkaline phosphatase, acid phosphatase, naphthol-AS-BI-phosphohydrolase, -glucosidase and -glucosidase, medium activity for esterase (C4), esterase lipase (C8) and leucine arylamidase, and strong activity for -galactosidase (API ZYM). Growth occurs in 0–5 % NaCl, with weak growth in 10 % NaCl. The G+C content of the strains is 59·4–60·4 mol%. Isolated from microbial mats from lakes Ace and Organic in the Vestfold Hills, Antarctica.
The type strain is LMG 21507T (=CIP 108322T).
Description of Loktanella fryxellensis sp. nov.
Loktanella fryxellensis (fry.xell.en'sis N.L. fem. adj. fryxellensis referring to the isolation source, Lake Fryxell, Antarctica).
Cells are Gram-negative, short rods (<1 µm by 2–3 µm), often forming pairs or short chains. Strains grow at 5–25 °C; optimal growth temperature is 25 °C but weak growth occurs at 30 °C. Pale-pink to beige, convex, translucent colonies with a diameter of 1 mm, with entire margins formed on marine agar plates after 6 days incubation. Growth also occurs on R2A agar, but the strains do not grow on nutrient agar or trypticase/soy agar, and colonies do not adhere to the agar. Degrades aesculin, Tween 80 and citrate (weak reaction). No growth is observed (API 20NE) on carbohydrates and acids are not produced from carbohydrates (API 20E). Agar, casein, DNA, gelatin, tyrosine and urea are not degraded. Tests for indole production, nitrate reduction, the Voges–Proskauer reaction and hydrogen sulfide production are negative. None of the strains shows activity for the enzymes arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase (API 20E) and lipase (C14), cystine arylamidase, -chymotrypsin, trypsin, -galactosidase, -glucuronidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase (API ZYM). Weak enzymic activity is observed for valine arylamidase, acid phosphatase, naphthol-AS-BI-phosphohydrolase and -glucosidase, medium activity for alkaline phosphatase, esterase (C4), esterase lipase (C8), -galactosidase and leucine arylamidase, and strong activity for -glucosidase (API ZYM). Growth occurs in 0–5 % NaCl but not in 10 % NaCl. The G+C content of the strains is 65·7–66·4 mol%. Isolated from microbial mats from Lake Fryxell, in the McMurdo Dry Valleys, Antarctica.
The type strain is LMG 22007T (=CIP 108323T).
Description of Loktanella vestfoldensis sp. nov.
Loktanella vestfoldensis (vest.fold.en'sis. N.L. fem. adj. vestfoldensis referring to the isolation source, lakes Ace and Pendant, Vestfold Hills, Antarctica).
Cells are Gram-negative, short rods (<1 µm by 3–4 µm), often forming pairs or short chains. Strains grow at 5–37 °C, but no growth is observed at 45 °C. Pale-pink, convex, translucent colonies with a diameter of <1 mm, with entire margins formed on marine agar plates. Growth also occurs on trypticase/soy agar (weak growth), nutrient agar (weak growth) and R2A agar. Colonies do not adhere to the agar. Degrades aesculin, Tween 80, citrate and urea. No growth is observed (API 20NE) on carbohydrates and acids are not produced from carbohydrates (API 20E). Agar, casein, DNA, gelatin, tyrosine and starch are not degraded. Tests for indole production, nitrate reduction, hydrogen sulfide production and the Voges–Proskauer reaction are negative. None of the strains shows activity for the enzymes arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase (API 20E) and lipase (C14), valine arylamidase, cystine arylamidase, -chymotrypsin, -galactosidase, -glucuronidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase (API ZYM). Weak enzymic activity is observed for alkaline phosphatase, leucine arylamidase, naphthol-AS-BI-phosphohydrolase, -galactosidase, -glucosidase and -glucosidase, medium activity for esterase (C4), esterase lipase (C8) and acid phosphatase, and strong activity for trypsin (API ZYM). Growth occurs in 0–5 % NaCl and weak growth in 10 % NaCl. The G+C content of the strains is 62·1–63·1 mol%. Isolated from microbial mats from lakes Ace and Pendant in the Vestfold Hills, Antarctica.
The type strain is LMG 22003T (=CIP 108321T).
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ACKNOWLEDGEMENTS |
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H.-Y. Weon, B.-Y. Kim, S.-H. Yoo, J.-S. Kim, S.-W. Kwon, S.-J. Go, and E. Stackebrandt Loktanella koreensis sp. nov., isolated from sea sand in Korea. Int J Syst Evol Microbiol, September 1, 2006; 56(Pt 9): 2199 - 2202. [Abstract] [Full Text] [PDF]
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Q. L. Wu, G. Zwart, M. Schauer, M. P. Kamst-van Agterveld, and M. W. Hahn Bacterioplankton Community Composition along a Salinity Gradient of Sixteen High-Mountain Lakes Located on the Tibetan Plateau, China Appl. Envir. Microbiol., August 1, 2006; 72(8): 5478 - 5485. [Abstract] [Full Text] [PDF]
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J.-C. Cho and S. J. Giovannoni Pelagibaca bermudensis gen. nov., sp. nov., a novel marine bacterium within the Roseobacter clade in the order Rhodobacterales. Int J Syst Evol Microbiol, April 1, 2006; 56(Pt 4): 855 - 859. [Abstract] [Full Text] [PDF]
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X. Dai, B.-J. Wang, Q.-X. Yang, N.-Z. Jiao, and S.-J. Liu Yangia pacifica gen. nov., sp. nov., a novel member of the Roseobacter clade from coastal sediment of the East China Sea. Int J Syst Evol Microbiol, March 1, 2006; 56(Pt 3): 529 - 533. [Abstract] [Full Text] [PDF]
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D. R. Arahal, M. C. Macian, E. Garay, and M. J. Pujalte Thalassobius mediterraneus gen. nov., sp. nov., and reclassification of Ruegeria gelatinovorans as Thalassobius gelatinovorus comb. nov. Int J Syst Evol Microbiol, November 1, 2005; 55(6): 2371 - 2376. [Abstract] [Full Text] [PDF]
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A. Buchan, J. M. Gonzalez, and M. A. Moran Overview of the Marine Roseobacter Lineage Appl. Envir. Microbiol., October 1, 2005; 71(10): 5665 - 5677. [Full Text] [PDF]
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E. P. Ivanova, N. V. Zhukova, A. M. Lysenko, N. M. Gorshkova, A. F. Sergeev, V. V. Mikhailov, and J. P. Bowman Loktanella agnita sp. nov. and Loktanella rosea sp. nov., from the north-west Pacific Ocean Int J Syst Evol Microbiol, September 1, 2005; 55(5): 2203 - 2207. [Abstract] [Full Text] [PDF]
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S. C. K. Lau, M. M. Y. Tsoi, X. Li, I. Plakhotnikova, M. Wu, P.-K. Wong, and P.-Y. Qian Loktanella hongkongensis sp. nov., a novel member of the {alpha}-Proteobacteria originating from marine biofilms in Hong Kong waters Int J Syst Evol Microbiol, November 1, 2004; 54(6): 2281 - 2284. [Abstract] [Full Text] [PDF]
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