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1 Department of Biochemistry and Plant Physiology, Faculty of Biology, Voronezh State University, Voronezh, Russia
2 All Russian Collection of Microorganisms (VKM), G. K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Moscow Region, 142290, Russia
3 Max-Planck-Institute for Marine Microbiology, Celsiusstraße 1, D-28359 Bremen, Germany
4 S. N. Winogradsky Institute of Microbiology of the Russian Academy of Sciences, Pr. 60-letiya Octyabrya 7/2, Moscow, 117811, Russia
Correspondence
Margarita Grabovich
margarita_grabov{at}mail.ru
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains D-419T, D-420, D-412T and D-416 are AY780905–AY780907 and AY780904, respectively.
Tables detailing the strains used in this study, the fatty acid profiles of strains and the DNA–DNA relatedness between strains and images showing the morphology of Giesbergeria voronezhensis sp. nov. and Giesbergeria kuznetsovii sp. nov. are available as supplementary material in IJSEM Online.
These authors contributed equally to the work. 
Present address: Department of Biology, Northeastern University, 360 Huntington Avenue, Boston, MA 02115, USA.
Present address: Bremen Institute for Materials Testing, Foundation Institute for Materials Science, Paul-Feller-Straße 1, D-28199 Bremen, Germany.
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; Pot et al., 1992; Sakane & Yokota, 1994; Hamana et al., 1994; Ding & Yokota, 2002). A combination of phylogenetic analysis and phenotypic/chemotaxonomic characterization for many Aquaspirillum species has resulted in the description of novel genera and/or novel species within the Alphaproteobacteria and Betaproteobacteria (Schleifer et al., 1991; Wen et al., 1999; Ding & Yokota, 2002; Cleenwerck et al., 2003).
We have isolated several heterotrophic, spiral-shaped strains from a number of freshwater habitats (Grabovich, 1984; Grabovich et al., 1987; Dubinina et al., 1993). Their phenotypic and genotypic properties led them to be classified as representatives of the genus Aquaspirillum (Grabovich et al., 1987; Dubinina et al., 1993). Strains D-419T, 420 and 424 were proposed as a novel species, ‘Aquaspirillum voronezhense’, and strain 412T was proposed as ‘Aquaspirillum kuznetsovi’, but these names have not been validly published (Grabovich et al., 1987, Dubinina et al., 1993). In this paper, we present the results of a polyphasic taxonomic study of freshwater spiral-shaped isolates and the revision of some closely related species previously belonging to the genus Aquaspirillum; [Aquaspirillum] giesbergeri, [Aquaspirillum] sinuosum, [Aquaspirillum] anulus, [Aquaspirillum] metamorphum and [Aquaspirillum] psychrophilum.
All strains used in this study are shown in Supplementary Table S1 (see supplementary data in IJSEM Online). Cultivation of the strains was carried out in a modified PSS medium (Caraway & Krieg, 1974) of the following composition (l–1), 1 g (NH4)2SO4, 1 g ammonium molybdate, 0·03 g CaCl2.2H2O, 1 g sodium succinate and 2 g peptone, at pH 7·0. Vitamins and microelements were added before inoculation (Pfennig & Lippert, 1966). The incubation temperature was 28 °C. The morphology of cells from 18 h cultures was studied with a phase-contrast microscope (NU–2; Zeiss) and in a transmission electron microscope (JEM-100C: JEOL) at an acceleration voltage of 80 kV. Preparations fixed with OsO4 were contrasted with a 2 % solution of NH4MoO4. Physiological and biochemical properties were determined as described previously (Dubinina et al., 1993). The ability to use different carbon and nitrogen sources was tested by removing peptone and succinate from the medium. Carbon and nitrogen sources were added to the medium at a concentration of 1 g l–1. The ability of the bacteria to utilize the test substrate was assayed after three reinoculations on the appropriate medium.
Isoprenoid quinones were extracted and purified as described previously (Collins & Jones, 1981). The fatty acid content was determined from 4–6 mg lyophilized biomass after acid methanolysis. Fatty acid methyl esters were analysed on a specialized chromatograph from the Microbial Identification System (Sherlock; MIDI Inc.) (Stead et al., 1992). DNA was isolated from 5 l batch cultures grown aerobically on modified PSS medium according to the method of Marmur (1961). The DNA G+C content was determined by thermal denaturation as described previously (Owen et al., 1976). DNA of Escherichia coli K-12 (=DSM 498) (51·7 mol%) was used as the reference. Levels of DNA–DNA binding were determined by measuring the renaturation rates of denatured DNA at the optimal renaturation temperatures as recommended by De Ley et al. (1970).
Almost-complete 16S rRNA gene sequences were amplified by PCR with the universal eubacterial primers 27f and 1492r and aligned using CLUSTAL_X software (Thompson et al., 1997). An evolutionary-distance matrix was calculated using the Jukes and Cantor algorithm (Jukes & Cantor, 1969). The phylogenetic tree was constructed using the neighbour-joining (Saitou & Nei, 1987) and maximum-parsimony (Fitch, 1971) methods. Bootstrap analyses were based on 1000 resamplings. The PAUP 4.0b10 (Swofford, 1998) and TREECON (Van de Peer & De Wachter, 1994) software packages were used for the analysis.
The nucleotide sequences for the 16S rRNA gene (1420–1460 nt) of isolates D-412T, D-419T, D-420 and D-416 were obtained. Phylogenetic analysis placed the studied strains within the family Comamonadaceae. The phylogenetic tree constructed using the neighbour-joining algorithm is shown in Fig. 1.
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The morphological and physiological properties of all studied strains are given in Tables 1, 2 and 3 and the species description. The cell morphology of two isolates can be seen in Supplementary Fig. S1 (see supplementary data in IJSEM Online).
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The high level of DNA–DNA hybridization (87–99 %) for strains D-419T, D-420 and D-424 indicates that the strains represent a single species (see Supplementary Table S3 in IJSEM Online). For strain D-419T and its close relatives (D-412T, [A.] anulus, [A.] giesbergeri and [A.] sinuosum), the DNA–DNA hybridization value was less than 39 %. Strain D-412T showed slightly higher values of DNA–DNA hybridization with the type strains of [A.] anulus, [A.] giesbergeri and [A.] sinuosum (36, 52 and 50 %, respectively). Although the 16S rRNA gene sequence of strain D-412T is almost identical to that of the type strain of [A.] annulus, its physiological properties are different (Table 1
). The ability to use additional organic compounds requires genes or complete pathways which might not be present in the type strain of [A.] annulus. This is also reflected in the low level of DNA–DNA hybridization between these two strains. The level of DNA–DNA hybridization between the three type strains of the Aquaspirillum species was 17–45 %. The high DNA–DNA hybridization value between strain D-416 and the type strain of [A.] metamorphum DSM 1837T (95 %) indicated that the strains represent a single species.
Polyphasic analysis demonstrates that isolate D-412T and strains D-419T, D-420 and D-424 are representatives of two separate species and are closely related to [A.] anulus, [A.] giesbergeri and [A.] sinuosum, which are misclassified species of the genus Aquaspirillum within the family Comamonadaceae (Wen et al., 1999; Ding & Yokota, 2002). Therefore, we propose to combine these species into a novel genus within the family Comamonadaceae, Giesbergeria gen. nov., with Giesbergeria voronezhensis sp. nov. as the type species. The type strain of G. voronezhensis is strain D-419T, with strains D-420 and D-424 as reference strains. Four other species of the genus are proposed, Giesbergeria kuznetsovii sp. nov. (type strain D-412T), Giesbergeria anulus comb. nov., Giesbergeria giesbergeri comb. nov. and Giesbergeria sinuosa comb. nov. The species of the novel genus can be differentiated from each other by phenotypic features (Table 1). Representatives of the novel genus differ from the recognized genera of the family Comamonadaceae in cell morphology and cell size, the spectrum of substrates used, fatty acid content and in an inability to perform denitrification (Tables 1 and 3).
The phylogenetic positions of [A.] metamorphum and [A.] psychrophilum indicate that both species are misclassified as members of the genus Aquaspirillum. The two species form a separate cluster (Fig. 1) from the genus Aquaspirillum and share different phenotypic and chemotaxonomic properties (Tables 2 and 3). Therefore, we propose to reclassify the two species into a novel genus, Simplicispira gen. nov., as Simplicispira metamorpha comb. nov. (the type species) and Simplicispira psychrophila comb. nov.
Description of Giesbergeria gen. nov.
Giesbergeria (Gies.ber.ger'i.a. N.L. fem. n. Giesbergeria named after the researcher G. Giesberger, who made a great contribution to the study of physiology of heterotrophic spirilla).
Gram-negative spiral cells. Cells are motile and have bipolar tufts of flagella. Cells accumulate poly-
-hydroxybutyric acid, some accumulate globules of elemental sulfur. Catalase- and oxidase-positive. Aerobes. Neutrophilic. Mesophilic. Do not grow with 3 % NaCl. Do not reduce nitrate to nitrite. Chemoorganoheterotrophs. Major fatty acids are 16 : 1 and 16 : 0. The latter acid may vary between representatives of the genus. The major respiratory ubiquinone is Q-8. The DNA G+C content is 56·5–60 mol%. The type species is Giesbergeria voronezhensis.
Description of Giesbergeria voronezhensis sp. nov.
Giesbergeria voronezhensis (vo.ro.nezh.en'sis. N.L. fem. adj. voronezhensis pertaining to Voronezh, the place from where the first strains were isolated).
Spiral cells, 1·3–2·1 µm in diameter, one to three helices, helix diameter 2·9–6·8 µm. Accumulates polyphosphate granules inside the cells and forms globules of elemental sulfur in the presence of sulfide. The pH for growth ranges from 6·0 to 9·0. The optimum growth temperature is 30 °C. Utilizes a wide range of organic acids for growth, including acetate, succinate, malate, fumarate, benzoate, isocitrate, formate, 2-oxoglutarate, oxaloacetate, pyruvate, salicylate, lactate and glyoxylate. Capable of growing on some amino acids as carbon sources. Does not utilize sugars or alcohols. Uses ammonium salts, casein hydrolysate, yeast extract, peptone, aspartate, glutamate and cysteine as nitrogen sources. Does not hydrolyse casein or starch. Does not use nitrates, sulfates, thiosulfate or fumarate as electron acceptors. Possesses urease activity. Forms hydrogen sulfide from cysteine. Does not form indole. Forms coloured products on a medium with benzoate. Predominant cellular fatty acids are 16 : 0, 16 : 1 and 14 : 0. The DNA G+C content is 58·5–60 mol%.
The type strain, D-419T (=DSM 12825T=CIP 107340T=VKM B-2350T), was isolated from active sludge from a wastewater aeration tank, Russia.
Description of Giesbergeria kuznetsovii sp. nov.
Giesbergeria kuznetsovii (kuz.net.so'vi.i. N.L. gen. n. kuznetsovii named after Sergey Kuznetsov, a Russian microbiologist who has made a great contribution to the study of microbial ecology).
Spiral cells, 1·2–1·5 µm in diameter, one to four helix loops, helix diameter 1·9–4·0 µm. Accumulates polyphosphate granules inside cells and forms globules of elemental sulfur in the presence of sulfide. The pH for growth ranges from 6·0 to 8·5. The optimum growth temperature is 28 °C. Utilizes a wide range of organic acids for growth, including acetate, succinate, malate, fumarate, benzoate, isocitrate, formate, 2-oxoglutarate, oxaloacetate, pyruvate, salicylate, lactate and glyoxylate. Uses the following alcohols: propanol, mannitol, glycerol, ethanol and butanol. Utilizes all tested amino acids. Does not utilize sugars. Uses ammonium salts, casein hydrolysate, yeast extract, peptone, aspartate, glutamate and cysteine as nitrogen sources. Does not hydrolyse casein or starch. Does not use nitrates, sulfates, thiosulfate or fumarate as electron acceptors. Possesses urease activity. Forms hydrogen sulfide from cysteine. Does not form indole. The predominant cellular fatty acids are 16 : 1 and 16 : 0. The DNA G+C content is 56·5 mol%.
The type strain, D-412T (=DSM 12827T=VKM B-2352T), was isolated from a sulfide spring, Russia.
Description of Giesbergeria sinuosa comb. nov.
Giesbergeria sinuosa (sin.u.o'sa. L. fem. adj. sinuosa sinuous, full of curves).
Basonym: Aquaspirillum sinuosum (Williams and Rittenberg 1957) Hylemon et al. 1973 (Approved Lists 1980).
The description is identical to the description given for Aquaspirillum sinuosum by Hylemon et al. (1973). In addition, the predominant cellular fatty acids are 16 : 1, 16 : 0, 17 : 1 and 18 : 1. The type strain is ATCC 9786T (=DSM 11556T).
Description of Giesbergeria giesbergeri comb. nov.
Giesbergeria giesbergeri (gies.ber'ge.ri. N.L. gen. n. giesbergeri of G. Giesberger, a researcher who made a great contribution to the study of heterotrophic spirilla).
Basonym: Aquaspirillum giesbergeri (Williams and Rittenberg 1957) Hylemon et al. 1973 (Approved Lists 1980).
The description is identical to that given for Aquaspirillum giesbergeri by Hylemon et al. (1973). In addition, the predominant cellular fatty acids are 16 : 1, anteiso-15 : 0, 16 : 0 and 18 : 1. The type strain is ATCC 11334T (=DSM 9157T=NCIB 9073T).
Description of Giesbergeria anulus comb. nov.
Giesbergeria anulus (an'u.lus. L. masc. n. anulus a ring).
Basonym: Aquaspirillum anulus (Williams and Rittenberg 1957) Hylemon et al. 1973 (Approved Lists 1980).
The description is identical to that given for Aquaspirillum anulus by Hylemon et al. (1973). In addition, the predominant cellular fatty acids are 16 : 0, 16 : 1 and 18 : 1. The type strain is ATCC 35958T (=NCIB 9012T).
Description of Simplicispira gen. nov.
Simplicispira (Sim.pli.ci.spi'ra. L. adj. simplex -icis simple; L. fem. n. spira a spiral; N.L. fem. n. Simplicispira a simple spiral).
Cells are polymorphic, weakly curved rods, spiral and motile by the use of bipolar tufts of flagella. Gram-negative. Cells accumulate poly--hydroxybutyric acid. Catalase- and oxidase-positive. Aerobes and facultative anaerobes; capable of denitrification. Neutrophilic. Mesophilic. Do not grow with 3 % NaCl. Chemoorganoheterotrophs. The major fatty acids are 16 : 0 and 16 : 1. The major respiratory ubiquinone is Q-8. The DNA G+C content is 63–65 mol%. The type species is Simplicispira metamorpha.
Description of Simplicispira metamorpha comb. nov.
Simplicispira metamorpha (me.ta.mor'pha. N.L. fem. adj. metamorpha changing).
Basonym: Aquaspirillum metamorphum (Terasaki 1961) Hylemon et al. 1973 (Approved Lists 1980).
The description is identical to that given for Aquaspirillum metamorphum by Hylemon et al. (1973). In addition, the predominant cellular fatty acids of the type strain are 16 : 0, 16 : 1 and 18 : 1. The reference strain D-416 (=DSM 12826) possesses urease activity and the predominant fatty acids are 16 : 0 and iso-16 : 1, but 15 : 0 and 17 : 0 have also been found. The type strain is ATCC 15280T (=DSM 1837T=NBRC 13960T).
Description of Simplicispira psychrophila comb. nov.
Simplicispira psychrophila (psy.chro.phi'la. Gr. adj. psychros cold; L. adj. philos loving; N.L. fem. adj. psychrophila cold-loving).
Basonym: Aquaspirillum psychrophilum (Terasaki 1973) Terasaki 1979 (Approved Lists 1980).
The description is identical to that given for Aquaspirillum psychrophilum by Hylemon et al. (1973). The type strain is DSM 11588T (=ATCC 33335T=NBRC 13611T=LMG 5408T).
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ACKNOWLEDGEMENTS |
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