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1 S. N. Winogradsky Institute of Microbiology, Russian Academy of Sciences, Prospect 60-letya Octyabrya 7/2, Moscow 117312, Russia
2 M. V. Lomonosov Moscow State University, Faculty of Biology Science, GSP-2, Leninskie Gory, Moscow 119992, Russia
3 Netherlands Institute of Ecology, 3631 AC Nieuwersluis, The Netherlands
4 Royal Netherlands Institute for Sea Research, Department of Marine Biogeochemistry and Toxicology, PO Box 59, 1790 AB Den Burg, The Netherlands
Correspondence
Svetlana N. Dedysh
dedysh{at}mail.ru
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ABSTRACT |
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7c; the major quinone is MK-6. The G+C content of the DNA is 54.4–56.5 mol%. Strains MPL7T, MOB77 and SB2 possess nearly identical 16S rRNA gene sequences and belong to the planctomycete lineage defined by the genus Planctomyces, being most closely related to Planctomyces limnophilus DSM 3776T (86.9–87.1 % sequence similarity). However, strain MPL7T showed only 28 % DNA–DNA hybridization with P. limnophilus DSM 3776T. Compared with currently described members of the genus Planctomyces, the isolates from northern wetlands do not form long and distinctive stalks, have greater tolerance of acidic conditions and low temperatures, are more sensitive to NaCl, lack pigmentation and degrade a wider range of biopolymers. The data therefore suggest that strains MPL7T, MOB77 and SB2 represent a novel genus and species, for which the name Schlesneria paludicola gen. nov., sp. nov., is proposed. Strain MPL7T (=ATCC BAA-1393T =VKM B-2452T) is the type strain of Schlesneria paludicola.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain MPL7T is AM162407.
Additional electron micrographs and temperature and pH growth profiles are available as supplementary material with the online version of this paper.
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; Schlesner & Stackebrandt, 1986; Staley et al., 1992; Fuerst, 1995, 2004, 2005; Ward et al., 2006). Originally described as freshwater organisms, members of this order were later shown to be ubiquitous in a wide range of aquatic and terrestrial environments with diverse conditions. Despite the reported widespread distribution, the known ecophysiological types of planctomycetes are quite limited. With the only exception of moderately thermophilic Isosphaera pallida (Giovannoni et al., 1987), all taxonomically described planctomycetes are both mesophilic and neutrophilic.
Until recently, there has been only one report on the isolation of a planctomycete-like strain from an acidic environment, i.e. peat bog water (pH 4.2) of the Kaltenhofer Moor near Kiel, Germany (Schlesner, 1994). This strain has not been described taxonomically, and no further information except a brief morphological characterization was given. We recently reported that planctomycetes represent one of the most numerous bacterial groups detectable by fluorescence in situ hybridization in acidic Sphagnum-dominated wetlands (Dedysh et al., 2006; Kulichevskaya et al., 2006; Ivanova & Dedysh, 2006). We have also reported the isolation of a few peat-inhabiting planctomycetes in pure culture (Dedysh et al., 2006; Kulichevskaya et al., 2006). One of these isolates, strain MPL7T, belonged to a phylogenetic lineage defined by the genus Planctomyces (Dedysh et al., 2006). The 16S rRNA gene sequence from isolate MPL7T showed 87 % similarity to that of the type strain of Planctomyces limnophilus (Hirsch & Müller, 1985), one of three cultured species of the genus Planctomyces. Later, we obtained two other isolates with similar morphology from Sphagnum peat. In this paper, we describe the characteristics and taxonomic position of these isolates from peat bogs.
Two strains, MPL7T and SB2, were isolated from acidic peat soil (pH 4.0) sampled at a depth of 10–20 cm (with a water table at approximately 15 cm depth) of the Sphagnum peat bog Bakchar, Tomsk region, western Siberia (5 ° 51' N 8 ° 50' E). Another strain, MOB77, was obtained from a peat sample (pH 4.2) collected from the upper (0–10 cm) oxic layer of the bog Obukhovskoe, Yaroslavl region, in European northern Russia (5 ° 14' N 3 ° 12' E). The isolation procedure and the culture conditions used were described elsewhere (Dedysh et al., 2006; Kulichevskaya et al., 2006). The isolates were maintained on agar medium M31 (modification of medium 31 described by Staley et al., 1992) containing (g per litre distilled water unless indicated) KH2PO4, 0.1; Hutner's basal salts, 20 ml; N-acetylglucosamine, 1.0; ampicillin sodium salt, 0.2; peptone, 0.1; yeast extract, 0.1; agar-agar (Difco), 18. The medium was adjusted to pH 5.8. Planctomyces limnophilus DSM 3776T (Hirsch & Müller, 1985) was used as a reference strain in our study. It was maintained on medium 621 recommended by the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ, Braunschweig, Germany) for cultivation of this bacterium.
Morphological observations and cell-size measurements were made with a Zeiss Axioplan 2 microscope and Axiovision 4.2 software (Zeiss). For negative staining, cells were dried onto grids and treated with 1 % (w/v) phosphotungstic acid. For the preparation of ultrathin sections, cells from 10-day-old cultures were fixed in 2 % (w/v) glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 6.8) for 0.5 h and then post-fixed in 1 % (w/v) osmium tetroxide in the same buffer for 4 h, dehydrated through an ethanol series and embedded in araldite. Thin sections were cut on an LKB-8800 ultratome and stained with lead citrate (Reynolds, 1963). Negatively stained cells and thin sections were examined with JEOL transmission electron microscopes JEM-100B and JEM-1011. For scanning electron microscopy, bacteria were fixed in 2 % (w/v) glutaraldehyde in liquid medium M31 without carbon sources for 0.5–1 h and in some cases post-fixed in 1 % (w/v) osmium tetroxide in the same medium for 4 h. The samples were then dehydrated through an ethanol series, left in absolute acetone overnight, critical-point-dried (Dryer HCP-2), coated with Au-Pd alloy (IB-3 Ion Coater) and examined with a JEOL JSM-6380LA scanning electron microscope.
Physiological tests were performed in liquid medium M31. Growth of strains MPL7T, MOB77 and SB2 was monitored by nephelometry at 600 nm in an Eppendorf BioPhotometer for 7–14 days under a variety of conditions, including temperatures of 4–37 °C, pH 3.8–8.0 and NaCl concentrations of 0–3.0 % (w/v). Variations in the pH were achieved by mixing 0.1 M solutions of H2SO4 and KOH. Carbon source utilization was determined using mineral medium MM supplemented with respective carbon sources (0.05 %, w/v). Medium MM contained (g per litre distilled water) KH2PO4, 0.1; (NH4)2SO4, 0.1; MgSO4 . 7H2O, 0.1; and 1 ml metal salt solution ‘44’ (Staley et al., 1992), the pH being adjusted to 5.5. Cultivation was done in 100 ml flasks containing 10 ml medium. Cultures were incubated at 25 °C for 2–3 weeks on a shaker. The capacity to degrade different biopolymers was examined by measuring the rate of CO2 production in tightly closed 120 ml serum bottles containing 10 ml liquid medium MM with 0.05 % (w/v) of the corresponding polymer substrate for 1 month at 20 °C. Control incubations were run in parallel under the same conditions but without substrate. Oxidative and fermentative utilization of carbohydrates was determined as described for the Hugh–Leifson test (Gerhardt et al., 1981). Nitrogen sources were tested using liquid MM medium with 0.05 % glucose in which (NH4)2SO4 was replaced with one of the following compounds at a concentration of 0.05 % (w/v): KNO3, KNO2, urea or one of the amino acids listed in Table 1. Gelatin liquefaction was assessed using ‘method 2’ described by Gerhardt et al. (1981) but, instead of mercury chloride, we used hot saturated ammonium sulfate. Susceptibility to antibiotics was determined on M31 agar plates using discs (Oxoid) containing the following antibiotics: ampicillin (10 µg), gentamicin (10 µg), kanamycin (30 µg), neomycin (10 µg), novobiocin (30 µg), streptomycin (10 µg), chloramphenicol (30 µg) and lincomycin (10 µg).
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, 2001). For phospholipid fatty acid (PLFA) analysis, the extract was fractionated on silicic acid into different polarity classes by sequential elution with chloroform, acetone and methanol. The methanol fraction containing the PLFA was derivatized using mild-alkaline methanolysis to yield fatty acid methyl esters (FAME). FAME standards of C12 : 0 and C19 : 0 were used for calculating retention indices and for quantification. Identification of FAMEs was based on retention time data against known standards. FAME concentrations were determined using a GC-FID system (Thermo Finnigan TRACE GC) equipped with a polar capillary column (SGE, BPX-70; 50 mx0.32 mmx0.25 µm) using the following oven conditions: initial temperature 50 °C for 1 min, increasing to 130 °C by 40 °C min–1 and then increasing to 230 °C by 3 °C min–1. To determine the double bond position of monounsaturated PLFAs, dimethyldisulfide (DMDS) derivatization was performed as described by Nichols et al. (1986). For neutral lipid analysis, the procedures described by Sinninghe Damsté et al. (2004) were used. Isoprenoid quinones were extracted according to Collins (1985) and analysed using a tandem-type mass spectrometer LCQ ADVANTAGE MAX and a Finnigan Mat 8430 ionization mass spectrometer.
Genomic DNA from the novel strains was extracted as described by Marmur (1961). The G+C content of DNA was determined by means of thermal denaturation using a Unicam SP1800 spectrophotometer at a heating rate of 0.5 °C min–1 and calculated according to Owen et al. (1969). DNA–DNA hybridization of strain MPL7T and P. limnophilus DSM 3776T was performed as described by De Ley et al. (1970). PCR-mediated amplification of the 16S rRNA gene from positions 28 to 1491 (numbering according to the International Union of Biochemistry nomenclature for Escherichia coli 16S rRNA) was performed using primers 9f and 1492r and reaction conditions described by Weisburg et al. (1991). 16S rRNA gene amplicons were purified using QIAquick spin columns (Qiagen) and sequenced on an ABI Prism 377 DNA sequencer using BigDye terminator chemistry, as specified by the manufacturer (PE Applied Biosystems). Phylogenetic analysis was carried out using the ARB program package (Ludwig et al., 2004).
Raised, opaque, uncoloured, small (1–2 mm), circular colonies with an entire edge and a smooth surface developed on agar medium M31 after incubation for 2 weeks at 24 °C. Four-week-old colonies were 2–3 mm in diameter. Mature cells of strains MPL7T, MOB77 and SB2 had an ellipsoid-like shape and were 1.3–2.1 µm long and 0.6–1.5 µm wide, being slightly larger than cells of P. limnophilus DSM 3776T (Table 1
). Cells occurred singly or in pairs or were arranged in rosettes (Fig. 1a), and reproduced by budding (Fig. 1b). The buds arose from the free cell pole of the mother cells. After separation, they displayed high motility due to the possession of subpolar flagella. In most cases, two flagella per cell were observed. Examination of thin sections revealed a characteristic type of cell organization in which a single membrane divides the cell into two major compartments (Fig. 1c). The nucleoid and most ribosomes were located in one of these compartments. This type of cell compartmentalization is characteristic of representatives of the genera Planctomyces and Pirellula (Lindsay et al., 2001; Fuerst, 2005; Ward et al., 2006). Examination of negatively stained cells using electron microscopy showed the presence of crateriform pits on the cell surface of the novel bacteria (Fig. 1d, e). These structures are highly characteristic of the planctomycete morphotype and displayed a polar distribution covering approximately one-third of the cell surface. We also observed an unusual spur-like projection on one pole of the cell, which gave the cell shape some similarity to a lemon (Fig. 1d). Similar spur-like projections have been observed before on cells of Planctomyces brasiliensis ATCC 49424T and Planctomyces sp. strain AGA/M18, isolated from the giant tiger prawn Penaeus monodon (Fuerst et al., 1997). Negative staining also revealed numerous, 4–8 nm thick, fimbria-like fibrillar structures (Supplementary Fig. S1A, available in IJSEM Online) as well as 10–15 nm thick fibrillar appendages (Supplementary Fig. S1B) on the cell surface of the novel strains. The fibrillar appendages developed more strongly when the cells were grown in liquid media with polymer growth substrates, such as chondroitin sulfate (Fig. 1h), and seem to play an important role in cell aggregation. Although formation of rosettes was commonly observed in cultures of the planctomycete-like isolates from peat bogs, we failed to discern the presence of stalks in these bacteria by observation with the phase-contrast microscope. When observed by the scanning electron microscope, the cells were seen to connect to each other by means of short stalk-like structures (Fig. 1g, h). Some of these structures resembled the bundles of twisted fibrils (Fig. 1g). This fibrillar material between cells arranged in pairs as well as the inner parts of cell rosettes was often covered by vesicle-like, electron-transparent bodies, 20–100 nm in diameter, that were seen on negatively stained cell preparations (Fig. 1e, f). The nature of these vesicle-like bodies remains unclear.
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), the novel isolates were also capable of fermenting carbohydrates. This trait might be of special importance for bacteria that inhabit wetlands. It also coincides well with our recent finding that planctomycetes are present in anoxic layers of the peat bog profile (Ivanova & Dedysh, 2006).
The list of carbon substrates tested in our experiments and the results are given in the species description and/or Table 1. In contrast to P. limnophilus DSM 3776T, the novel isolates from Sphagnum peat did not assimilate galactose or raffinose, but assimilated fucose and salicin and were able to degrade a wider range of biopolymers. In addition to chondroitin sulfate, pullulan, gelatin and xylan, hydrolysed by P. limnophilus DSM 3776T, strains MPL7T, MOB77 and SB2 were capable of hydrolysing fucoidan, laminarin, aesculin and pectin. All three novel isolates displayed catalase and cytochrome oxidase activities, but urease activity was absent. Dissimilatory nitrate reduction was positive. Growth factors were not required, but yeast extract increased the growth rate slightly. Ammonia, nitrate, N-acetylglucosamine, Bacto peptone, Bacto yeast extract, alanine, aspartate, glutamine and threonine were utilized as nitrogen sources. All three novel strains were resistant to ampicillin, streptomycin, chloramphenicol, lincomycin and novobiocin, but were sensitive to neomycin, kanamycin and gentamicin.
Strains MPL7T, MOB77 and SB2 grew in the pH range 4.2–7.5, with an optimum at pH 5.0–6.2 (Supplementary Fig. S2A). The temperature range for growth was 4–32 °C, with an optimum at 15–26 °C (Supplementary Fig. S2B). Growth was inhibited completely at NaCl concentrations above 0.5 % (w/v). Thus, compared with P. limnophilus DSM 3776T, the isolates from northern wetlands had greater tolerance of acidic conditions and low temperatures and were more sensitive to NaCl (Table 1).
Similar to other described planctomycetes (Sittig & Schlesner, 1993; Ward et al., 2006), our isolates contained menaquinone-6 (MK-6) as the predominant isoprenoid quinone. The cellular fatty acid compositions of strains MPL7T, MOB77 and SB2 displayed significant similarity to that of P. limnophilus DSM 3776T (Table 2). Similar to the latter species, the major components of the PLFA profile of the novel strains were C16 : 0 and C16 : 17c fatty acids. However, compared with P. limnophilus DSM 3776T, the PLFA profiles of our isolates had double the content of C16 : 17c and much lower contents of C18 : 19c. A high content of C18 : 19c, which is not normally a major component in bacteria, was earlier regarded as a feature specific to members of Planctomyces and Pirellula (Kerger et al., 1988). Our study shows that not all planctomycetes possess significant amounts of this PLFA. The neutral lipid compositions of strains MPL7T, MOB77 and SB2 (Table 3) were highly similar and resembled that of P. limnophilus DSM 3776T. All of these organisms contained a n-C31 polyunsaturated alkene (9–10 double bonds) previously detected in Antarctic bacteria (Nichols et al., 1995) and a novel series of C24–C30 
,(–1) diols. Compared with P. limnophilus DSM 3776T, the novel strains contained much lower levels of C24–C26 alkan-1-ols, but higher levels of hop-22(29)-ene. The latter was previously detected in other planctomycetes (Sinninghe Damsté et al., 2004). This chemotaxonomic similarity supports the phylogenetic relationships outlined below.
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). The three novel strains possessed nearly identical (99.8–99.9 % similarity) 16S rRNA gene sequences. The closest phylogenetic relatives (97.5–97.8 % sequence similarity) were two strains of taxonomically uncharacterized planctomycetes, Planctomyces sp. strains Schlesner 638 and 642, which were isolated from a compost leakage water (Ward et al., 1995). The closest taxonomically described organism was P. limnophilus DSM 3776T (86.9–87.1 % sequence similarity). The level of 16S rRNA gene similarity between the novel isolates and the other cultured species of the genus Planctomyces, Planctomyces maris and P. brasiliensis, was 83.6–85.6 %.
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). The DNA–DNA hybridization value of strain MPL7T with P. limnophilus DSM 3776T was 28 %. This low level of genomic DNA relatedness suggests the differentiation of the novel strains at the genus level, which is also supported by the results of fatty acid analysis and a number of physiological tests.
We therefore propose that strains MPL7T, MOB77 and SB2 should be classified as representatives of a novel genus and species, for which the name Schlesneria paludicola gen. nov., sp. nov. is proposed. Compared with representative of the genus Planctomyces members of this novel taxon have greater tolerance of acidic conditions and low temperatures, are more sensitive to NaCl, lack pigmentation and degrade a wider range of biopolymers (Table 4).
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Ellipsoid-like cells that occur singly or in pairs or are arranged in rosettes. Encapsulated. Reproduce by budding. Buds arise from the free cell pole of the mother cells. Adult cells are immobile. Daughter cells are motile by means of two subpolar flagella. Cells are connected to each other by means of numerous fibrillar appendages. Stalk-like structures are short and rarely observed. Colonies are small and uncoloured. Chemo-organotrophic facultative aerobes. Possess weak hydrolytic capabilities. Catalase- and cytochrome oxidase-positive, but urease-negative. Dissimilatory nitrate reduction is positive. Moderately acidophilic and mesophilic. Sensitive to NaCl. The major quinone is MK-6. The major fatty acids are C16 : 0 and C16 : 17c; the major neutral lipids are n-C31 polyunsaturated alkenes, n-C26-2,25-diols and n-C24-2,23-diols. The genus is a member of the phylum ‘Planctomycetes’, order Planctomycetales, family Planctomycetaceae. The type species is Schlesneria paludicola.
Description of Schlesneria paludicola sp. nov.
Schlesneria paludicola (pa.lu.di'co.la. L. n. palus -udis a marsh, bog; L. suff. -cola inhabitant, dweller; N.L. n. paludicola a bog-dweller).
Displays the properties given in the genus description. Mature cells are 1.3–2.1 µm long and 0.6–1.5 µm wide. Free cell poles are covered with crateriform pits and possess an unusual spur-like projection, which gives rise to a cell shape with some similarity to a lemon. Carbon sources (0.05 %, w/v) include glucose, N-acetylglucosamine, cellobiose, maltose, sucrose, trehalose, fucose and salicin. Cannot utilize fructose, galactose, raffinose, rhamnose, sorbose, ribose, glycerol, methanol, ethanol, glucuronic acid, acetate, benzoate, caproate, citrate, fumarate, glutarate, lactate, malate, pyruvate, succinate, propionate, mannitol, tartrate, alanine, arginine, asparagine, aspartate, cysteine, cystine, glutamine, glycine, histidine, isoleucine, leucine, lysine, methionine, norleucine, ornithine, phenylalanine, proline, serine, threonine, tryptophan, tyrosine or valine. Capable of hydrolysing fucoidan, laminarin, aesculin, pectin, chondroitin sulfate, pullulan, gelatin and xylan. Cannot hydrolyse starch, lichenan or chitin. Nitrogen sources (0.05 %, w/v) include ammonia, nitrate, N-acetylglucosamine, Bacto peptone, Bacto yeast extract, alanine, aspartate, glutamine and threonine. Vitamins are not required. Resistant to ampicillin, streptomycin, chloramphenicol, lincomycin and novobiocin, but sensitive to neomycin, kanamycin and gentamicin. Capable of growth at pH 4.2–7.5 (optimum pH 5.0–6.2) and at 4–32 °C (optimum 15–26 °C). NaCl inhibits growth at concentrations above 0.5 % (w/v). The G+C content of the DNA varies between 54.4 and 56.5 mol% (56.3 mol% for the type strain). Acidic wetlands are the only known habitat.
The type strain is strain MPL7T (=VKM B-2452T =ATCC BAA-1393T), which was isolated from the Sphagnum peat bog Bakchar, Tomsk region, western Siberia.
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ACKNOWLEDGEMENTS |
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