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Bereich Mikrobiologie, Ludwig-Maximilians-Universität München, Maria-Ward-Str. 1a, D-80638 München, Germany
Correspondence
Jörg Overmann
j.overmann{at}lrz.uni-muenchen.de
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ABSTRACT |
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-4 subgroup of the Proteobacteria were isolated from freshwater lakes using a high-throughput cultivation technique. The non-motile and slender rod-shaped cells formed orange–red-pigmented colonies. The main carotenoids were nostoxanthin and keto-nostoxanthin. According to the absorption spectrum, two different photosynthetic light-harvesting complexes, an LHI complex and a B800-830-type peripheral LHII complex, were present in the cells. The predominant fatty acids of strain so42T were hexadecenoic acid (16 : 1
7c) and octadecenoic acid (18 : 17c), whereas 17 : 16c and 14 : 0 iso 2-OH were present in smaller amounts. The main polar lipids were phosphatidylethanolamine, phosphatidylglycerol, phosphatidylcholine, diphosphatidylglycerol, glycolipid and sphingoglycolipids. The major respiratory lipoquinone was ubiquinone-10, whereas ubiquinone-9 was present in smaller amounts. The three strains were cytochrome oxidase-negative and catalase-positive and formed alkaline and acid phosphatases. The strains grew chemoorganoheterotrophically in mineral media supplemented with various organic acids, amino acids or complex substrates such as peptone and yeast extract. The G+C content of the genomic DNA of strain so42T was 64·3 mol%. The three novel isolates contained the same 16S rRNA gene sequence. The 16S rRNA gene sequence similarity to the closest phylogenetic relative Sandaracinobacter sibiricus was only 92·8 %. Accordingly, the three strains represent a new genus and species, for which the name Sandarakinorhabdus limnophila gen. nov., sp. nov., is proposed, with strain so42T (=DSM 17366T=CECT 7086T) as the designated type strain.
Published online ahead of print on 16 December 2005 as DOI 10.1099/ijs.0.63970-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain so42T is AY902680.
A table detailing the substrate utilization patterns of strains so36, so42T and wo26 is available as supplementary material in IJSEM Online.
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; Allgaier et al., 2003; de la Torre et al., 2003). Despite their broad geographical distribution, the ecology and biogeochemical significance of aerobic, anoxygenic, phototrophic bacteria have only been studied in the marine environment, where they can constitute 10–30 % of the total bacterial community and account for up to 5 % of the photosynthetic electron transport (Shiba et al., 1991; Kolber et al., 2001; Béjà et al., 2002). In comparison, much less is known about the diversity and function of this bacterial group in freshwater lakes (Kolber et al., 2000; Page et al., 2004). Until very recently, freshwater representatives of aerobic, anoxygenic, phototrophic bacteria had been isolated exclusively from nutrient-rich sediment environments (Yurkov & Beatty, 1998), such as cyanobacterial mats in warm or hot springs (Sandaracinobacter, Erythromonas, Erythromicrobium, Roseococcus and Porphyrobacter) or from the surfaces of subtropical ponds (Porphyrobacter), river water (Roseateles) and acidic mineral environments and mine drainages (Acidiphilium and Acidisphaera). All planktonic species of marine and freshwater, aerobic, phototrophic bacteria isolated to date are affiliated with either the Rhodobacteraceae (-3 subgroup of the Proteobacteria) or the 
-1 subgroup of the Proteobacteria (Yurkov, 2001). Very recently, however, two planktonic BChl a-containing species (Rhodobacter sp. HTCC515 and the betaproteobacterium HTCC528) were isolated from the ultraoligotrophic Crater Lake, OR, USA (Page et al., 2004). Freshwater environments may therefore harbour a greater diversity and abundance of aerobic, anoxygenic, phototrophic bacteria than that appreciated to date.
In the present study, we describe the first phototrophic, planktonic freshwater species representing a novel lineage within the -4 subgroup of the Proteobacteria to be isolated in pure culture. The novel phylotype was also detected in situ by PCR-denaturing gradient gel electrophoresis fingerprinting in a previous study (Gich et al., 2005). Dot-blot hybridization with genomic probes demonstrated that the isolates constitute 0·5–2·3 % of the natural bacterioplankton community (Gich et al., 2005). Furthermore, the 16S rRNA gene sequence of the isolates was detected in lakes of all trophic states (oligotrophic to eutrophic) (Gich et al., 2005). The novel type of bacterium thus appears to represent a typical and widely distributed constituent of freshwater bacterioplankton. Future studies will reveal whether aerobic, anoxygenic, phototrophic bacteria of the 4-subgroup of the Proteobacteria are of significance for the carbon cycle in freshwater lakes.
Bacterial strains were isolated from the mesotrophic prealpine Starnberger See (25 km south-west of Munich, Germany) and from the oligotrophic alpine Walchensee (near Garmisch-Partenkirchen, 50 km south of Munich), as described previously (Bruns et al., 2003; Gich et al., 2005). Purification of the colonies was performed on agar plates containing synthetic freshwater medium and a ten-vitamin mixture (Bartscht et al., 1999) and 1 % (w/v) peptone. Cell morphology was examined by using an inverse phase-contrast microscope (Axiovert 200; Zeiss). The three isolates grew as single cells and formed orange–red-pigmented colonies with a smooth surface on synthetic freshwater agar medium. Colonies of strain so42T were bigger (1–3 mm) than those of strains so36 and wo26 (usually 
0·5 mm). In addition, the colonies of strain so42T had a mucilaginous texture because of the production of extracellular slime. The strains could be stored at –80 °C in 50 % glycerol or 7 % DMSO for at least 7 months. The cells were non-motile rods and reproduced by binary fission (Fig. 1a). During exponential growth, cells were 0·32±0·09x1·55±0·44 µm (strain so36), 0·31±0·06x0·80±0·19 µm (strain so42T) and 0·26±0·05x2·33±0·83 µm (strain wo26) (Table 1). Cells of strain so42T elongated upon entry into the stationary phase (Fig. 1b), becoming 0·24±0·03x3·24±0·81 µm. No change in cell volume occurred upon transfer of cultures from low-nutrient artificial freshwater medium to media containing high concentrations of complex substrates. Electron microscopy of ultrathin sections indicated that the cells possessed a typical Gram-negative cell wall (Fig. 1c). No intracytoplasmic membrane systems were detected. Many cells contained a single electron-dense polar granule, most probably consisting of polyphosphate.
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) were similar for all three strains and exhibited maxima at 430–490 and 800–865 nm, indicating the presence of carotenoids and BChl a, respectively. Absorption maxima at 800 and 865 nm and the shoulder at 837 nm (Fig. 2b) are characteristic for two different photosynthetic, light-harvesting complexes, LHI (865 nm) and a B800-830-type LHII (800–837 nm). LHII is present in only a few and very distantly related aerobic phototrophic bacteria, namely Erythromicrobium ramosum, ‘Erythromicrobium ezovicum’ and ‘Erythromicrobium hydrolyticum’, and is missing from Sandaracinobacter sibiricus and other species (Yurkov et al., 1997; Yurkov & Beatty, 1998). Because the novel type of bacterium was found in lakes of all trophic states, the presence of a photosynthetic apparatus is not simply an adaptation to oligotrophic environments. This is supported by the observation that the isolates grew in mineral media supplemented with up to 1 % peptone and hence are not obligate oligotrophs. Carotenoid analysis was performed by HPLC according to method B of Airs et al. (2001). Individual carotenoids were identified according to their retention time and absorption spectra by co-chromatography of pigment extracts of the reference strains Erythrobacter longus DSM 6997T and Erythromicrobium ramosum DSM 8510T. The strains contained BChl a esterified with phytol (BChl aP). Based on HPLC analyses, three major carotenoids were present. All three strains contained nostoxanthin as a major carotenoid. Strains so36 and wo26 had an almost identical pigment composition and contained keto-nostoxanthin as a second major carotenoid. In addition, the three strains contained two unidentified carotenoids that are novel among the aerobic, anoxygenic phototrophic bacteria, an unidentified carotenoid containing a keto group (
max=590 nm) resembling bacteriorubixanthinal and a cis-isomer of this unidentified carotenoid.
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, b). Polar lipid analyses were carried out by the Identification Services and B. J. Tindall, DSMZ. For fatty acid analysis, 40 mg (wet weight) of cells was scraped from Petri dishes and the fatty acid methyl esters were extracted by using the method of Miller (1982) and Kuykendall et al. (1988). DNA G+C content was analysed according to Mesbah et al. (1989). The polar lipid fingerprints of the isolates so36, so42T and wo26 obtained by two-dimensional TLC were similar to those of Sphingomonas phyllosphaerae FA2T (Rivas et al., 2004) and were identified by their chromatographic behaviour and staining characteristics (Fig. 3). The fatty acid composition is summarized in Table 2. Interestingly, only one saturated fatty acid without hydroxy groups was detected in strain so42T (16 : 0), whereas a variety of saturated fatty acids are commonly found in the alphaproteobacteria (Denner et al., 2002; Rainey et al., 2003; Yoon et al., 2003, 2004). The similarity index of the fatty acid patterns of strain so42T and the closest related species present in the MIDI database, Novosphingobium aromaticivorans F199T, was 0·04. Since a similarity value of >0·30 is indicative of strains belonging to the same species, the fatty acid analyses provide independent evidence for an isolated phylogenetic position of the three strains.
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). Strains so36, so42T and wo26 were Gram-negative and tested negative for cytochrome oxidase and were catalase-positive. Enzymic activities were determined with the API ZYM test system (bioMérieux), according to the manufacturer's protocol. The three isolates produced the same spectrum of enzyme activities (Table 3) except for trypsin and -galactosidase, which were only detected as weak activities in the isolates so42T and wo26, respectively. The three isolates showed a strong positive reaction in tests for alkaline and acid phosphatases, which is consistent with an adaptation to limiting phosphate concentrations in Walchensee and Starnberger See (Chróst, 1991; Gich et al., 2005).
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). The isolates grew as obligately aerobic chemoorganoheterotrophs. Fermentation or anaerobic growth with nitrate or sulfate were not detected. However, the three strains differed with respect to carbon utilization (see Supplementary Table S1 in IJSEM Online). Since our strains were isolated from oligotrophic freshwater lakes with low organic carbon content, two concentrations of fatty acids and complex substrates were tested with respect to possible inhibition of growth. All three strains grew readily with crotonate, protocatechuate and valerate, but did not utilize most alcohols (nine of ten) or sugars (29 of 31) tested. The only commonly used sugar and amino acid in all three strains were glucose and (+)-L-cysteine, respectively. Strain so36 did not use any of the tested oxo-acids. All three strains were capable of growing on complex organic substrates such as Casamino acids, yeast extract and peptone, but no growth was observed when fermented rumen extract was used, even at low concentrations (0·001 %). Maximum growth rates were achieved for all three strains at 0·1 % [460 (mg C) l–1] yeast extract. Strains so42T and wo26 showed a higher tolerance towards peptone [maximum growth rates observed at 1 % peptone, corresponding to 4·3 g (mg C) l–1], whereas the maximum growth rate of strain so36 was observed at 0·1 % peptone [0·4 (g C) l–1]. The minimum doubling times recorded for the strains were between 12·1 and 16·8 h. When precultures grown at low substrate concentrations were inoculated into these complex media with high substrate concentrations, lag phases of up to 80 h occurred.
The 16S rRNA genes were amplified for each of the three strains using primers 8f and 1492r (Lane, 1991). The PCR products were separated from free PCR primers, purified using the QIAquick Spin kit (Qiagen) and sequenced directly employing eight primers to cover the entire 16S rRNA gene (Gich et al., 2005), using an ABI Prism BigDye Terminator cycle sequencing ready reaction kit (Applied Biosystems) and an ABI Prism 310 Genetic Analyzer (Applied Biosystems). Sequences were analysed using the ARB software package (Ludwig et al., 2004). Additional sequences of close relatives of other more recently described BChl a-containing alphaproteobacteria present in GenBank were retrieved from the database employing BLAST 2.0.4 (Altschul et al., 1997) and imported into the ARB database. The Fast Aligner V1.03 tool was used for automatic sequence alignment with previously aligned sequences from the ARB database. The alignment was subsequently checked and corrected manually based on secondary-structure information. Phylogenetic trees were constructed using maximum-likelihood and neighbour-joining methods and bootstrap values were calculated to determine the robustness of the clusters. Sequence similarities were calculated using the ARB distance matrix. A comparison of the almost-complete 16S rRNA gene sequences (positions 60–1458, Escherichia coli numbering) revealed that all three isolates contained identical sequences. Maximum-likelihood and neighbour-joining analyses led to the same results (Fig. 4). Based on the phylogenetic analysis, the isolates belong to the family Sphingomonadaceae, with Sandaracinobacter sibiricus strain RB16-17T, an aerobic BChl a-containing bacterium that forms an isolated phylogenetic branch among non-photosynthetic members of the -4 subgroup of the Proteobacteria, representing the most closely related species with a validly published name. The latter was isolated from a microbial mat in freshwater near hydrothermal sulfide-containing vents on the bottom of the Bol'shoi river (Yurkov & Gorlenko, 1990). The sequence similarity of isolates so36, so42T and wo26 to Sandaracinobacter sibiricus was 92·8 %, which clearly indicates an independent phylogenetic lineage. A 16S rRNA gene sequence divergence of 3 % is commonly used as a criterion for the separation of two bacterial species (Stackebrandt & Goebel, 1994). Bacterial genera typically show 93 % sequence similarity of the 16S rRNA gene. Numerous cytological, biochemical and physiological characteristics (Table 1
) support the conclusion that the three isolates represent a novel bacterial genus. Accordingly, a new genus and species, Sandarakinorhabdus limnophila gen. nov., sp. nov., is proposed. Genomic fingerprints generated with ERIC-PCR or repetitive extragenic palindromic DNA (REP)-PCR primers (de Bruijn, 1992) ranged from 6000 to 400 bp (Fig. 5). According to both analyses, strains so36 and wo26 are more similar to each other than to strain so42T.
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Cells are non-spore-forming, non-motile rods that do not form a capsule and are Gram-negative. They reproduce by binary fission and form orange–red-pigmented colonies with smooth surfaces on agar plates. Cells may contain polyphosphate granules and exhibit strong enzymic activity for acid and alkaline phosphatases. Cytochrome oxidase-negative and catalase-positive. Obligately aerobic chemoorganoheterotrophs. Fermentation or anaerobic growth with nitrate or sulfate are not detected. Produce Bchl a. Grow in the presence of a number of short-chain organic acids and amino acids as electron donors and carbon sources. Grow well in media containing 0·1 % peptone or yeast extract. 16S rRNA gene sequence information places the genus within the -4 subgroup of the Proteobacteria, with Sandaracinobacter as its phylogenetic neighbour. The type species is Sandarakinorhabdus limnophila.
Description of Sandarakinorhabdus limnophila sp. nov.
Sandarakinorhabdus limnophila [lim.no'phi.la. Gr. n. limnos (or limnè) lake, pool of standing water; Gr. adj. philos loving; N.L. fem. adj. limnophila lake-loving, isolated from a freshwater lake].
General characteristics are the same as those given in the description of the genus. Rods are 0·31±0·06x0·80±0·19 µm with a biovolume of 0·08 µm3. Facultatively oligotrophic, grows as single cells and forms orange–red colonies of 1–3 mm with mucilaginous texture on agar plates. Cells absorb at 430–490 nm and at 800, 837 and 865 nm, because of the presence of carotenoids and BChl aP, respectively. Nostoxanthin is the main carotenoid. In addition, two unidentified carotenoids containing keto groups are present. Keto-nostoxanthin may also be present in some strains. Contains two different light-harvesting complexes (LHI and LHII). Grows well in media containing up to 1 % peptone. Major fatty acids of the cellular lipids are hexadecenoic acid (16 : 17c) and octadecenoic acid (18 : 17c). Predominant glycolipids are phosphatidylethanolamine, phosphatidylglycerol, phosphatidylcholine, diphosphatidylglycerol, glycolipid and two sphingoglycolipids. The respiratory lipoquinones are ubiquinone-10 (92 %) and ubiquinone-9 (8 %). The G+C content of the genomic DNA is 64·3 mol% (determined by HPLC).
The type strain is so42T (=DSM 17366T=CECT 7086T), which was isolated from the mesotrophic freshwater lake Starnberger See (Bavaria, Germany).
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ACKNOWLEDGEMENTS |
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50 % are depicted. Sequences included in cluster 